A LysM Receptor Heteromer Mediates Perception of Arbuscular Mycorrhizal Symbiotic Signal in Rice Mol. Plant (IF 10.812) Pub Date : 2019-11-06 Jiangman He, Chi Zhang, Huiling Dai, Huan Liu, Xiaowei Zhang, Jun Yang, Xi Chen, Yayun Zhu, Dapeng Wang, Xiaofeng Qi, Weichao Li, Zhihui Wang, Guoyong An, Nan Yu, Zuhua He, Yong-Fei Wang, Youli Xiao, Peng Zhang, Ertao Wang
Symbiotic microorganisms improve nutrient uptake by plants. To initiate mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, plants perceive Myc factors, including lipochitooligosaccharides (LCOs) and short-chain chitooligosaccharides (CO4/CO5), secreted by AM fungi. However, the molecular mechanism of Myc factors perception remains elusive. Here, we identified a heteromer of LysM receptor-like kinases, OsMYR1/OsLYK2 and OsCERK1, that mediates perception of AM fungi in rice. CO4 directly binds to OsMYR1, promoting the dimerization and phosphorylation of this receptor complex. Compared to control plants, Osmyr1 and Oscerk1 mutant rice plants are less sensitive to Myc factors and show decreased AM colonization. We engineered transgenic rice by expressing chimeric receptors that respectively replaced the ectodomains of OsMYR1 and OsCERK1 with those from the homologous Nod factor receptors MtNFP and MtLYK3 of Medicago truncatula. Transgenic plants displayed increased calcium oscillations in response to Nod factors compared to control rice. Our findings reveal a mechanism for mycorrhizal symbiotic signal perception in rice, and the ectopic expression of chimeric Nod/Myc receptors achieves a potentially important step towards generating cereals that host nitrogen-fixing bacteria.
Arabidopsis ECAP is a New Adaptor Protein that Connects JAZ Repressors with TPR2 Co-repressor to Suppress Jasmonate-Responsive Anthocyanin Accumulation Mol. Plant (IF 10.812) Pub Date : 2019-11-06 Changjiang Li, Lei Shi, Yanan Wang, Wei Li, Binqing Chen, Lei Zhu, Ying Fu
Suppression mechanisms employed by transcriptional repressors commonly exist in diverse phytohormone signaling pathways. In Arabidopsis thaliana, JASMONATE-ZIM DOMAIN (JAZ) proteins are transcriptional repressors that function as negative regulators of diverse JA responses. Novel Interactor of JAZ (NINJA) is an adaptor protein connecting JAZs with the co-repressor, TOPLESS (TPL), to mediate gene repression in JA-dependent root growth inhibition and defense pathways. However, whether NINJA or other adaptor proteins are employed in other JA responsive biological processes remains to be elucidated. In the present study, we demonstrate that a previously uncharacterized protein, ECAP (EAR motif-Containing Adaptor Protein), directly interacts with JAZ6/8 and enhances their transcriptional repression activities. We also provide evidence that ECAP is a novel adaptor protein for JAZ6/8 recruitment of the transcriptional co-repressor, TPR2, into a transcriptional repressor complex, to repress the WD-repeat/bHLH/MYB complex, an important transcriptional activator in the JA-dependent anthocyanin biosynthesis pathway. This novel insight, together with previous studies, reveals that specific adaptor proteins are critical for distinct JA responses by pairing different JAZs (which possess overlapping but also individual functions) with the general co-repressors, TPL and TPRs.
Phytosphinganine Affects Plasmodesmata Permeability via Facilitating PDLP5-Stimulated Callose Accumulation in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-11-04 Liu Ning-Jing, Zhang Tao, Liu Zhao-Hui, Chen Xin, Guo Hui-Shan, Ju Bai-Hang, Zhang Yuan-Yuan, Li Guo-Zhu, Zhou Qiang-Hui, Qin Yong-Mei, Zhu Yu-Xian
Plant plasmodesmata (PDs) are specialized channels that enable communication between neighboring cells. The intercellular permeability of PDs affecting plant development, defense and responses to stimulus must be tightly regulated. Analysis of specific PD membrane lipid composition and their impact on PD permeability will provide new insights into PD regulatory mechanism. Herein, we report that the Arabidopsis sld1 sld2 double mutant, lacking sphingolipid long-chain base 8 desaturases 1 and 2, displayed decreased PD permeability due to a significant increase in callose accumulation. Plasmodesmata-located protein 5 (PDLP5) was significantly enriched in the leaf epidermal cells of sld1 sld2 and showed specific binding affinity to phytosphinganine (t18:0), suggesting that the enrichment of t18:0-based sphingolipids in sld1 sld2 PDs might facilitate the recruitment of more PDLP5. The double mutants showed enhanced resistance to the fungal-wilt pathogen Verticillium dahlia or the bacterium Peudomonas syringae pv tomato DC3000. This phenotype was fully restored in sld1 sld2 pdlp5. Thus, we proposed that phytosphinganine might regulate PDs functions and cell-to-cell communication by modifying the level of PDLP5 in PD membranes.
A Transcriptional Network Promotes Anthocyanin Biosynthesis in Tomato Flesh Mol. Plant (IF 10.812) Pub Date : 2019-11-01 Chuanlong Sun, Lei Deng, Minmin Du, Jiuhai Zhao, Qian Chen, Tingting Huang, Hongling Jiang, Chang-Bao Li, Chuanyou Li
Dietary anthocyanins are important health-promoting antioxidants that make a major contribution to the quality of fruits. It is intriguing that most tomato cultivars do not produce anthocyanins in fruit. However, the purple tomato variety Indigo Rose, which combines the dominant Aft locus and the recessive atv locus from wild tomato species, exhibits light-dependent anthocyanin accumulation in the skin. Here, we report that whereas Aft encodes a functional allele of an anthocyanin activator named SlAN2-like, atv encodes a non-functional allele of the anthocyanin repressor SlMYBATV. The expression of SlAN2-like is responsive to light and a functional SlAN2-like can activate both anthocyanin biosynthetic genes and their regulatory genes, suggesting that SlAN2-like acts as a master regulator and plays a critical role for the activation of anthocyanin biosynthesis. Our results reveal that cultivated tomatoes contain a non-functional allele of this master regulator and therefore fail to produce anthocyanins. Indeed, expression of a functional SlAN2-like in a tomato cultivar led to the activation of the entire anthocyanin biosynthesis pathway and high levels of anthocyanin accumulation in both peel and flesh. Our study exemplifies that efficient engineering of complex metabolic pathways could be achieved through tissue-specific expression of master transcriptional regulators.
Light triggers the miRNA-biogenetic inconsistency for de-etiolated seedling survivability in Arabidopsis thaliana Mol. Plant (IF 10.812) Pub Date : 2019-10-31 Suk Won Choi, Moon Young Ryu, András Viczián, Hyun Ju Jung, Gu Min Kim, Agustin L. Arce, Natalia P. Achkar, Pablo Manavella, Ulla Dolde, Stephan Wenkel, Attila Molnár, Ferenc Nagy, Seok Keun Cho, Seong Wook Yang
The shift of dark-grown seedlings into light causes enormous transcriptome changes followed by a dramatic developmental transition. Here, we show that miRNA biogenesis also undergoes regulatory changes during de-etiolation. Etiolated seedlings maintain low levels of primary-miRNAs (pri-miRNAs) and miRNA processing core proteins, such as Dicer-like 1 (DCL1), SERRATE (SE) and HYPONASTIC LEAVES 1 (HYL1), whereas during de-etiolation, both pri-miRNAs and the processing components accumulated to high levels. However, most miRNA levels did not notably increase in response to light. To reconcile this inconsistency, we demonstrate that an unknown suppressor decreases miRNA-processing activity and light-induced SMALL RNA DEGRADING NUCLEASE 1 (SDN1) shortens the half-life of several miRNAs in de-etiolated seedlings. Taken together, we suggest a novel mechanism, miRNA-biogenetic inconsistency, which accounts for the intricacy of miRNA biogenesis during de-etiolation. This mechanism is essential for the survival of de-etiolated seedlings after long-term skotomorphogenesis and their optimal adaptation to ever-changing light conditions.
Genetic contribution of paleopolyploidy to adaptive evolution in angiosperms Mol. Plant (IF 10.812) Pub Date : 2019-10-31 Shengdan Wu, Baocai Han, Yuannian Jiao
Ancient whole-genome duplications (WGD or polyploidy) are prevalent in plants, and some WGDs occurred during the timing of severe global environmental changes. It has been suggested that WGDs may have contributed to plant adaptation. However, it still lacks of empirical evidence from genetic level to support the hypothesis. Here, we investigated the survivors of gene duplicates from multiple ancient WGD events on the major branches of angiosperm phylogeny, and aimed to explore genetic evidence supporting the significance of polyploidy. Duplicated genes co-retained from three waves of independent WGDs (∼120 million years ago (Ma), ∼66 Ma and <20 Ma) were investigated in 25 selected species. Gene families functioning in low temperature and darkness were commonly retained gene duplicates after the eight independently occurred WGDs in many lineages around the Cretaceous–Paleocene (K-Pg) boundary, when the global cooling and darkness were the two main stresses. Moreover, the commonly retained duplicates could be key factors which may have contributed to the robustness of the critical stress related pathways. In addition, genome-wide transcription factors (TFs) functioning in stresses tend to retain duplicates after waves of WGDs, and the co-selected gene duplicates in many lineages may play critical roles during severe environmental stresses. Finally, our results shed new light on the significant contribution of paleopolyploidy to plant adaptation during global environmental changes in the evolutionary history of angiosperms.
Genome-wide dissection of co-selected UV-B responsive pathways in the UV-B adaptation of qingke Mol. Plant (IF 10.812) Pub Date : 2019-10-26 Xingquan Zeng, Hongjun Yuan, Xuekui Dong, Meng Peng, Xinyu Jing, Qijun Xu, Tang Tang, Yulin Wang, Sang Zha, Meng Gao, Congzhi Li, Chujin Shu, Zexiu Wei, Wangmu Qimei, Yuzhen Basang, Jiabu Dunzhu, Zeqing Li, Lijun Bai, Tashi Nyima
Qingke (Tibetan hulless barley) has long been cultivated and exposed to long-term and strong UV-B radiation on the Tibetan Plateau, which renders it an ideal target for elucidating novel UV-B responsive mechanisms. Here we report a comprehensive metabolite profiling and metabolite-based genome-wide association study using 196 diverse qingke and barley accessions. Our results demonstrated both constitutive and induced accumulation, and common genetic regulation, of metabolites of the different phenylpropanoid branches in UV-B protection. A total of 90 significant mGWAS loci for these metabolites were located in the barley-qingke differentiation regions and a number of high-level metabolite trait alleles were found to be significantly enriched in qingke, suggesting co-selection of various phenylpropanoids. Upon dissecting the entire phenylpropanoid pathway, we identified a number of determinants controlling natural variation of phenylpropanoid contents, including three novel proteins, a flavone C-pentosyltransferase, a tyramine hydroxycinnamoyl acyltransferase and a MYB transcription factor. Our study, furthermore, demonstrated co-selection of both constitutive and induced phenylpropanoids for UV-B protection in this species.
Discriminated sgRNAs-based SurroGate System Greatly Enhances the Screening Efficiency of Plant Base-edited Cells Mol. Plant (IF 10.812) Pub Date : 2019-10-18 Wen Xu, Yongxing Yang, Ya Liu, Guiting Kang, Feipeng Wang, Lu Li, Xinxin Lv, Si Zhao, Shuang Yuan, Jinling Song, Ying Wu, Feng Feng, Xiaoqing He, Chengwei Zhang, Wei Song, Jiuran Zhao, Jinxiao Yang
The development of CRISPR/Cas9-mediated base editing has made genomic modification more efficient. However, selecting genetically modified cells from millions of treated cells, especially plant cells, is still challenging. In this study, an efficient surrogate reporter system was established in rice to enrich base-edited cells based on a defective hygromycin resistance gene. After step-by-step optimization, the Discriminated sgRNAs-based SurroGate system (DisSUGs) was generated by artificially differentiating editing abilities using wild-type sgRNA to target the surrogate reporter gene and enhanced sgRNA to target endogenous sites. The DisSUGs enhanced the screening efficiency of base-edited cells by 3- to 5-fold for a PmCDA1-involved cytosine-to-tyrosine base editor (PCBE), and 2.5- to 6.5-fold for an adenine base editor (ABE) at endogenous targets. These targets showed editing efficiencies of <25% in the conventional system. The DisSUGs greatly enhanced the frequency of homozygous substitutions and expanded the activity window slightly for both a PCBE and an ABE. Analyses of the total number of single nucleotide variants from whole genome sequencing revealed that, compared with the non-enriched PCBE strategy, the DisSUGs did not alter the frequency of genome-wide sgRNA-independent off-target mutations, but slightly increased the frequency of target-dependent off-target mutations. Collectively, DisSUGs in this study greatly enhances the screening efficiency of plant base-edited cells and will be an useful system in the future application.
YR36/WKS1-mediated Phosphorylation of PsbO, an Extrinsic Member of Photosystem II, Inhibits Photosynthesis and Confers Stripe Rust Resistance in Wheat Mol. Plant (IF 10.812) Pub Date : 2019-10-14 Shuai Wang, Qiu-Ping Li, Jianfeng Wang, Yan Yan, Guo-Liang Zhang, Yan Yan, Huifei Zhang, Jiajie Wu, Feng Chen, Xiaojie Wang, Zhensheng Kang, Jorge Dubcovsky, Jin-Ying Gou
Wheat stripe rust, due to infection by Puccinia striiformis f. sp. tritici (Pst), is a devastating disease that is causing significant global grain yield losses. Yr36, which encodes the Wheat Kinase START1 (WKS1), is an effective high-temperature adult-plant resistance gene and confers resistance to a broad spectrum of Pst races. We previously showed that WKS1 phosphorylates the thylakoid ascorbate peroxidase (tAPX) protein and reduces its ability to detoxify peroxides, which may contribute to the accumulation of reactive oxygen species (ROS). WKS1-mediated Pst resistance is accompanied by leaf chlorosis in the Pst-infected regions, but the underlying mechanisms remain still elusive. Here, we show that WKS1 interacts with and phosphorylates PsbO, an extrinsic member of photosystem II (PSII), to reduce photosynthesis and regulate leaf chlorosis in conferring Pst resistance. A point mutation in PsbO-A1 or reductions in its transcript levels by RNA interference resulted in chlorosis and reduced Pst sporulation. Biochemical analyses revealed that WKS1 phosphorylates PsbO at two conserved amino acids involved in its physical interactions with PSII and reduces the binding affinity of PsbO to PSII. Phosphorylated PsbO dissociated from the PSII protein complex, and underwent fast degradation by cysteine and aspartic proteases. Taken together, these results demonstrate that perturbations of wheat PsbO by point mutation or its phosphorylation by WKS1 reduce photosynthesis rate and delays the growth of Pst pathogen before the induction of ROS.
Vascular cambium-localized AtSPDT mediates xylem-to-phloem transfer of phosphorus for its preferential distribution in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-10-11 Guangda Ding, Gui Jie Lei, Naoki Yamaji, Kengo Yokosho, Namiki Mitani-Ueno, Sheng Huang, Jian Feng Ma
Recent progress has shown that the preferential distribution of mineral nutrients is mediated by node-based transporters in gramineous plants, but it is poorly understood for the mechanisms of preferential distribution in dicots. Here, we report a distinct mechanism for the preferential distribution of phosphorus (P) through detailed functional analysis of AtSPDT/AtSULTR3;4 (SULTR-like P Distribution Transporter) in Arabidopsis. AtSPDT is a homolog of rice OsSPDT and localized to the plasma membrane. It also showed proton-dependent transport activity for P. AtSPDT was mainly expressed in rosette basal region and leaf petiole and its expression was up-regulated by P-deficiency. Tissue-specific analysis showed that AtSPDT was mainly located at the vascular cambium of different organs, as well as in the parenchyma tissues of both xylem and phloem region. Knockout of this gene inhibited the growth of new leaves under low P due to decreased P distribution to those organs. The seed yield was similar between mutant lines and wild type, but the mutant lines contained 8.2%-33.6% less P in seeds. These results indicate that AtSPDT localized at the vascular cambium is involved in the preferential distribution of P to the developing tissues through the xylem-to-phloem transfer mainly in rosette basal region and leaf petiole.
CURLY LEAF regulates micro RNA activity by controlling ARGONAUTE 1 degradation in plants Mol. Plant (IF 10.812) Pub Date : 2019-10-10 Delfina A. Ré, Damian A. Cambiagno, Agustin L. Arce, Ariel H. Tomassi, Marisol Giustozzi, Paula Casati, Federico D. Ariel, Pablo A. Manavella
CURLY LEAF (CLF) encodes the methyl-transferase sub-unit of the Polycomb Repressor Complex 2 (PRC2), which regulates the expression of target genes through H3K27 tri-methylation. We isolated a new CLF mutant allele (clf-78) using a genetic screening designed to identify micro RNAs (miRNA) deficient mutants. CLF mutant plants showed impaired miRNA activity caused by increased AGO1 ubiquitination and enhanced degradation in specific tissues. Such CLF-mediated AGO1 regulation was evidenced when plants were exposed to UV radiation, causing increased susceptibility of clf mutants to some UV-induced responses. Furthermore, we showed that CLF directly regulates FBW2, which in turn triggers AGO1 degradation in the mutants. Interestingly, AGO1 bound to a target appeared particularly prone to degradation in the mutant plants, a process that is exacerbated when the complex bound a non-cleavable target. Thus, a prolonged AGO1-target interaction seems to favor AGO1 degradation, suggesting that non-cleavable miRNA targets may overcome translation inhibition by modulating AGO1 stability in plants.
Stripe Rust Effector PstGSRE1 Disrupts Nuclear Localization of ROS-Promoting Transcription Factor TaLOL2 to Defeat ROS-Induced Defense in Wheat Mol. Plant (IF 10.812) Pub Date : 2019-10-10 Tuo Qi, Jia Guo, Peng Liu, Fuxin He, Cuiping Wan, Md Ashraful Islam, Brett M. Tyler, Zhensheng Kang, Jun Guo
Puccinia striiformis f. sp. tritici (Pst), a biotrophic plant pathogen, secretes numerous effectors to modulate host defense systems. Understanding the molecular mechanisms of Pst effectors that regulate wheat immunity is of great importance for the development of novel strategies for durable control of stripe rust. In this study, we identified a glycine-serine-rich effector gene, PstGSRE1, which is highly induced during early infection. Transgenic expression of PstGSRE1 RNAi constructs in wheat significantly reduced virulence of Pst and increased H2O2 accumulation in wheat. PstGSRE1 was shown to target the ROS-associated transcription factor TaLOL2, a positive regulator of wheat immunity. PstGSRE1 disrupted the nuclear localization of TaLOL2 and suppressed ROS-mediated cell death induced by TaLOL2, thus compromising host immunity. This work reveals a novel strategy that rust fungi exploit effectors to modulate host defense and facilitate pathogen infection.
Translational Regulation of Metabolic Dynamics during Effector-Triggered Immunity Mol. Plant (IF 10.812) Pub Date : 2019-09-27 Heejin Yoo, George H. Greene, Meng Yuan, Guoyong Xu, Derek Burton, Lijing Liu, Jorge Marqués, Xinnian Dong
Recent studies have shown that global translational reprogramming is an early activation event in pattern-triggered immunity, when plants recognize microbe-associated molecular patterns. However, it is not fully known whether translational regulation also occurs in subsequent immune responses, such as effector-triggered immunity (ETI). In this study, we performed genome-wide ribosome profiling in Arabidopsis upon RPS2-mediated ETI activation and discovered that specific groups of genes were translationally regulated, mostly in coordination with transcription. These genes encode enzymes involved in aromatic amino acid, phenylpropanoid, camalexin, and sphingolipid metabolism. The functional significance of these components in ETI was confirmed by genetic and biochemical analyses. Our findings provide new insights into the diverse translational regulation in the plant immune responses and demonstrate that translational coordination of metabolic gene expression is an important strategy for ETI.
A PIF7-CONSTANS-Centered Molecular Regulatory Network Underlying the Shade-Accelerated Flowering Mol. Plant (IF 10.812) Pub Date : 2019-09-27 Renshan Zhang, Chuanwei Yang, Yupei Jiang, Lin Li
To compete with their neighbors for light and escape shaded environments, sun-loving plants have developed shade avoidance syndrome (SAS) to alter plant architecture and initiate early flowering and seed set. Previous studies on SAS mainly focused on dissecting the molecular basis of hypocotyl elongation in seedlings under shade light, however, the molecular mechanisms underlying the shade-accelerated flowering in adult plants remain unknown. Here, we found that CONSTANS (CO) and PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) have an additive effect on shade-induced flowering, but LONG HYPOCOTYL IN FAR-RED1 (HFR1) represses early flowering through binding to CO and PIF7 and preventing the binding of CO to the promoter of FLOWERING LOCUS T (FT) and the binding of PIF7 to the promoter of pri-MIR156E/F. Under shade, dephosphorylated PIF7 and accumulated CO, balanced by HFR1, up-regulate the expression of FT, TSF, SOC1 and SPLs and result in accelerated flowering. Moreover, the function of PIF7 in flowering time is independent of phyA. These regulatory interactions establish a crucial link between the light signal and the genetic network that regulates flowering transition under shade.
Control of Bird Feeding Behavior by Tannin1 through Modulating the Biosynthesis of Polyphenols and Fatty Acid-Derived Volatiles in Sorghum Mol. Plant (IF 10.812) Pub Date : 2019-09-23 Peng Xie, Jiayang Shi, Sanyuan Tang, Chengxuan Chen, Aimal Khan, Fengxia Zhang, Ying Xiong, Chao Li, Wei He, Guodong Wang, Fumin Lei, Yaorong Wu, Qi Xie
Bird predation during seed maturation causes great loss to agricultural production. In this study, through GWAS analysis of a large-scale sorghum germplasm diversity panel, we identified that Tannin1, which encodes a WD40 protein functioning in the WD40/MYB/bHLH complex, controls bird feeding behavior in sorghum. Metabolic profiling analysis showed that a group of sorghum accessions preferred by birds contain mutated tan1-a/b alleles and accumulate significantly lower levels of anthocyanins and condensed tannin compounds. In contrast, a variety of aromatic and fatty acid-derived volatiles accumulate at significantly higher levels in these bird-preference accessions. We subsequently conducted both sparrow feeding and sparrow volatile attractant assays, which confirmed, respectively, the antifeedant and attractant functions of these differentially accumulated metabolites. In addition, the connection between the biosynthesis pathway of anthocyanin and proanthocyanidin and the pathway of fatty acid–derived volatile biosynthesis was demonstrated by discovering that Tannin1 complex modulates fatty acid biosynthesis by regulating the expression of SbGL2 in sorghum, thus affecting the accumulation of fatty acid-derived volatiles. Taken together, our study identified Tannin1 as the gene underlying the major locus controlling bird feeding behavior in sorghum, illustrating an example of the identification of an ecologically impactful molecular mechanism from field observation and providing significant insights into the chemistry of bird–plant ecological interactions.
LORELEI-LIKE GPI-ANCHORED PROTEINS 2/3 regulate pollen tube growth as chaperones and coreceptors for ANXUR/BUPS receptor kinases in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-09-18 Hanqian Feng, Chen Liu, Rong Fu, Minmin Zhang, Hui Li, Lianping Shen, Qiqi Wei, Xiang Sun, Lin Xu, Bin Ni, Chao Li
Pollen tube growth is crucial for successful fertilization. In Arabidopsis thaliana, the ANXUR (ANX)/BUPS receptor kinase complex controls and maintains pollen tube growth in response to autocrine RAPID ALKALINIZATION FACTOR4/19 (RALF4/19) signaling; however, the molecular and cellular mechanisms underlying the ANX/BUPS-mediated regulation of pollen tube growth are unexplored. Here, we found that pollen-specific LORELEI-LIKE GPI-ANCHORED PROTEINS 2 and 3 (LLG2/3) promoted pollen tube growth in vitro and in vivo. LLG2/3 interacted with ANX/BUPS in a RALF4-concentration-dependent manner, suggesting that ANX/BUPS-LLG2/3 might act as a receptor–coreceptor complex. Inhibiting the ANX/BUPS-LLG2/3 interaction led to the cytoplasmic retention of ANX1/2, in both knockdown llg2/3 mutants and in anx1/2 mutants lacking the J region, which is the LLG2/3 interaction site. Moreover, we found that RALF4 induced the production of reactive oxygen species (ROS) and that stimulated the pollen tube growth and reduced the pollen burst rate. However, we observed reduced ROS levels in the pollen tubes of the LLG2/3-RNAi lines, and application of exogenous H2O2 rescued the defective pollen tube growth phenotypes. Our study highlights LLG2/3 as novel regulatory components of pollen tube growth that chaperone ANX/BUPS for secretion to the apical plasma membrane and act as coreceptors of ANX/BUPS in the activation of ROS production.
Local changes in chromatin accessibility and transcriptional networks underlying the nitrate response in Arabidopsis roots Mol. Plant (IF 10.812) Pub Date : 2019-09-14 José M. Alvarez, Tomás C. Moyano, Tao Zhang, Diana E. Gras, Francisco J. Herrera, Viviana Araus, José A. O’Brien, Laura Carrillo, Joaquín Medina, Jesús Vicente-Carbajosa, Jiming Jiang, Rodrigo A. Gutiérrez
Transcriptional regulation, determined by chromatin structure and regulatory elements interacting at promoter regions, is a key step in plant responses to environmental cues. Nitrate (NO3-) is a nutrient signal that regulates the expression of hundreds of genes in Arabidopsis thaliana. Here we integrate mRNA-seq, genome-wide RNA polymerase II (RNPII), ChIP-Seq and DNase-seq data sets to establish the relationship between RNPII occupancy and chromatin accessibility in response to NO3- treatments in Arabidopsis root organs. Genomic footprinting allowed us to identify in vivo regulatory elements controlling gene expression in response to NO3- treatments. NO3--modulated TF footprints are important for a rapid increase in RNPII occupancy and transcript accumulation over time. We mapped key TF regulatory interactions and functionally validated the role of NAP, a NAC-domain containing TF, as a new regulatory factor in NO3- transport. Our strategy provides a comprehensive view of transcriptional networks in response to a nutrient signal in Arabidopsis roots.
A Molecular Framework for the Control of Adventitious Rooting by the TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-09-11 Abdellah Lakehal, Salma Chaabouni, Emilie Cavel, Rozenn Le Hir, Alok Ranjan, Zahra Raneshan, Ondřej Novák, Daniel I. Păcurar, Irene Perrone, François Jobert, Laurent Gutierrez, Laszlo Bakò, Catherine Bellini
In Arabidopsis thaliana, canonical auxin-dependent gene regulation is mediated by 23 transcription factors from the AUXIN RESPONSE FACTOR (ARF) family interacting with 29 auxin/indole acetic acid repressors (Aux/IAA), themselves forming coreceptor complexes with one of six TRANSPORT INHIBITOR1/AUXIN-SIGNALLING F-BOX (TIR1/AFB) PROTEINS. Different combinations of co-receptors drive specific sensing outputs, allowing auxin to control a myriad of processes. Considerable efforts have been made to discern the specificity of auxin action. However, owing to a lack of obvious phenotype in single loss-of-function mutants in Aux/IAA genes, most genetic studies have relied on gain-of-function mutants, which are highly pleiotropic. ARF6 and ARF8 are positive regulators of adventitious root initiation upstream of jasmonate, but the exact auxin co-receptor complexes controlling the transcriptional activity of these proteins was still unknown. Here using loss-of-function mutants we show that IAA6, IAA9 and IAA17 genes act additively in the control of AR initiation, and by performing protein-protein interaction analysis, we show that the corresponding proteins interact with ARF6 and/or ARF8 and likely repress their activity. We also demonstrate that TIR1 and AFB2 are positive regulators of adventitious root formation and suggest a dual role for TIR1 in the control of JA biosynthesis and conjugation, as revealed by upregulation of several JA biosynthesis genes in the tir1-1 mutant. We propose that in the presence of auxin, TIR1 and AFB2 form specific sensing complexes with IAA6, IAA9 and/or IAA17 that modulate JA homeostasis to control AR initiation.
Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-binding Elements of Multiple Susceptibility Genes in Rice Mol. Plant (IF 10.812) Pub Date : 2019-09-04 Zhengyin Xu, Xameng Xu, Qiang Gong, Ziyang Li, Ying Li, Sai Wang, Yangyang Yang, Wenxiu Ma, Longyu Liu, Bo Zhu, Lifang Zou, Gongyou Chen
Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial blight of rice, recruits transcription activator-like effectors (TALEs) to induce expression of OsSWEET genes, which function in sugar transport and disease susceptibility (S). To engineer broad-spectrum bacterial blight resistance, we used CRISPR/Cas9-mediated gene editing to disrupt the TALE-binding elements (EBEs) of two S genes, OsSWEET11 and OsSWEET14, in rice cv. Kitaake, which harbors recessive resistance allele of Xa25/OsSWEET13. The engineered rice line MS14K exhibited broad-spectrum resistance to most Xoo strains with a few exceptions, suggesting that the compatible strains may contain new TALEs. We identified Tal5LN18 and Tal7PXO61, two types of PthXo2-like TALEs, as major virulence factors in the compatible Xoo strains LN18 and PXO61, respectively, and found that Xoo encodes at least five types of PthXo2-like effectors. Given that PthXo2/PthXo2.1 target OsSWEET13 for transcriptional activation, the genomes of 3000 rice varieties were analyzed for EBE variations in OsSWEET13 promoters, and ten Xa25-like haplotypes were identified. Tal5LN18 and Tal7PXO61 were shown to bind slightly different EBE sequences in the OsSWEET13 promoter and activated its expression. CRISPR/Cas9 technology was then used to generate InDels in the EBE of the OsSWEET13 promoter in the mutant MS14K. This resulted in the creation of new germplasm with three edited OsSWEET EBEs and broad-spectrum resistance against all Xoo strains tested. Our findings illustrate how to disarm TALE-S co-evolved loci to generate broad-spectrum resistance through the loss of effector-triggered susceptibility in plants.
Rheostatic control of ABA signaling through HOS15-mediated OST1 degradation Mol. Plant (IF 10.812) Pub Date : 2019-09-03 Akhtar Ali, Jae Kyoung Kim, Masood Jan, Haris Ali Khan, Irfan Ullah Khan, Mingzhe Shen, Junghoon Park, Chae Jin Lim, Shah Hussain, Dongwon Baek, Kai Wang, Woo Sik Chung, Vicente Rubio, Sang Yeol Lee, Zhizhong Gong, Woe Yeon Kim, Ray A. Bressan, Jose M. Pardo, Dae-Jin Yun
Dehydrating stresses trigger the accumulation of abscisic acid (ABA), a key plant stress-signaling hormone that activates Snf1-Related Kinases (SnRK2s) to mount adaptive responses. However, the regulatory circuits that terminate the SnRK2s signal relay after acclimation or post-stress conditions remain to be defined. Here, we show that the desensitization of the ABA-signal is achieved by the regulation of OST1 (SnRK2.6) protein stability via the E3-ubiquitin-ligase HOS15. Upon ABA signal, HOS15-induced degradation of OST1 is inhibited and stabilized OST1 promotes the stress-response. When the ABA signal terminates, protein phosphatases ABI1/2 promote the rapid degradation of OST1 via HOS15. Notably, we found that even in the presence of ABA, OST1 levels were also depleted within hours of ABA signal onset. The unexpected dynamics of OST1 abundance was resolved by a systematic mathematical modeling demonstrating a desensitizing feedback loop by which OST1-induced up-regulation of ABI1/2 leads to the degradation of OST1. This model illustrates the complex rheostat dynamics underlying the ABA-induced stress response and desensitization.
Type-II Metacaspases Mediate the Processing of Plant Elicitor Peptides in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-08-24 Wenzhong Shen, Jiuer Liu, Jian-Feng Li
Plants can produce animal cytokine-like immune peptides, among which the plant elicitor peptides (Peps) derive from the C-termini of their precursors (PROPEPs). Recently, the functions of Peps have been expanded beyond immunity. However, a long-standing enigma is how PROPEPs are processed into Peps. Here, we report that the Ca2+-dependent type-II metacaspases (MCs) constitute the proteolytic enzymes to mediate PROPEP processing in Arabidopsis. In protoplasts, co-expression of PROPEP1 with type-II MCs, including MC4 to MC9, can promote the generation of processed Pep1. Destruction of the catalytic cysteine residue in MC4 or the conserved arginine residue preceding the Pep1 sequence blocks PROPEP1 cleavage, whereas the bacterial elicitor flg22 can enhance the MC4-mediated PROPEP1 processing. MC4 can cleave PROPEP1 in vitro and also cleave PROPEP2 to PROPEP8, but, surprisingly, not PROPEP6 in protoplasts. Domain swapping between PROPEP1 and PROPEP6 suggests a hidden role of the sequence context upstream of the Pep sequence for PROPEP processing. Flg22-induced PROPEP1 processing and Botrytis cinerea resistance are severely impaired in the mc4/5/6/7 quadruple mutant plants. Taken together, our findings reveal the type-II MCs as new players in Pep signaling, and lay the foundation for understanding the regulation of multifaceted functions of Peps in plant immunity and beyond.
Blue Light Triggered-Chemical Reactions Underlie Phosphate Deficiency-induced Inhibition of Root Elongation of Arabidopsis Seedlings Grown in Petri Dishes Mol. Plant (IF 10.812) Pub Date : 2019-08-13 Zai Zheng, Zhen Wang, Xiaoyue Wang, Dong Liu
To tolerate phosphate (Pi) deficiency in the environment, plants alter their developmental and metabolic programs. In studying the molecular mechanism underlying root developmental responses to Pi deficiency, researchers have extensively used Petri dish-grown seedlings of the model plant Arabidopsis (Arabidopsis thaliana). A typical developmental response of the Petri-dish grown Arabidopsis seedlings to Pi deficiency is the inhibition of primary root (PR) growth. This response is generally thought to enhance the production of lateral roots and root hairs, which increases the plant’s ability to obtain Pi and is therefore regarded as an active cellular response. Here, we report that direct illumination of the root surface with blue light is critical and sufficient for the Pi deficiency-induced inhibition of PR growth of Arabidopsis seedlings. We further show that a blue light-triggered malate-mediated photo-Fenton reaction and a Fenton reaction form a Fe redox cycle in the root apoplast. This Fe redox cycle results in the production of hydroxyl radicals that inhibit PR growth. In addition to revealing the molecular mechanism underlying Pi deficiency-induced inhibition of Arabidopsis PR growth, our work demonstrated that this developmental change is not an active cellular response; instead, it is a phenotype resulting from growth in transparent Petri dishes. This finding is significant because illuminated, transparent Petri dishes have been routinely used to study Arabidopsis root responses to environmental changes.
Inositol Pyrophosphate InsP8 Acts as an Intracellular Phosphate Signal in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-08-13 Jinsong Dong, Guojie Ma, Liqian Sui, Mengwei Wei, Viswanathan Satheesh, Ruyue Zhang, Shenghong Ge, Jinkai Li, Tong-En Zhang, Christopher Wittwer, Henning J. Jessen, Huiming Zhang, Guo-Yong An, Dai-Yin Chao, Dong Liu, Mingguang Lei
The maintenance of cellular phosphate (Pi) homeostasis is of great importance in living organisms. The SPX domain-containing proteins, SPX1, from both Arabidopsis and rice have been proposed to act as sensors of Pi status. The molecule signaling the cellular Pi status to regulate Pi homeostasis in plants, however, remains to be identified, as Pi itself does not bind to the SPX domain. Here, we report the identification of the inositol pyrophosphate InsP8 as a signaling molecule that regulates Pi homeostasis in Arabidopsis. Polyacrylamide gel electrophoresis profiling of InsPs revealed that InsP8 level positively correlates with cellular Pi concentration. We demonstrated that the homologs of diphosphoinositol pentakisphosphate kinase PPIP5K, VIH1 and VIH2, function redundantly to synthesize InsP8, and the vih1 vih2 double mutants over-accumulate Pi. SPX1 directly interacts with PHR1, the central regulator of Pi starvation responses, to inhibit its function under Pi-replete condition. However, this interaction is compromised in vih1 vih2 double mutant, resulting in the constitutive induction of Pi starvation-induced genes, indicating that plant cells cannot sense cellular Pi status without InsP8. Furthermore, InsP8 can directly bind to the SPX domain of SPX1 and is essential for the interaction between SPX1 and PHR1. Our study revealed that InsP8 acts as the ligand that binds to the intracellular Pi sensor SPX1 to control Pi homeostasis in plants.
DELLA and EDS1 Form A Feedback Regulatory Module to Fine-tune Plant Growth-Defense Tradeoff in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-08-02 Yuge Li, Yuhua Yang, Yilong Hu, Hailun Liu, Ming He, Ziyin Yang, Fanjiang Kong, Xu Liu, Xingliang Hou
Plants maintain a dynamic balance between growth and defense when encountering constant pathogen infections, thus optimizing allocation of resource for survival. However, the detailed regulatory mechanism, especially in response to biotrophic bacterial infection, remains elusive. Here, we demonstrate that DELLA proteins and the essential resistance regulator EDS1 function as a central module in modulating plant growth-defense tradeoff via direct interaction. When infected by Pst DC3000, EDS1 rapidly promotes SA biosynthesis and resistance-related genes expression to prime defense response, while pathogen infection stabilizes DELLA proteins RGA and RGL3 to restrict growth in an EDS1-partially dependent manner, which benefits the resistance to pathogens. However, increasingly accumulated DELLAs interact with EDS1 to suppress SA overproduction and excessive resistance response. Our findings reveal a DELLA-EDS1-mediated feedback regulatory loop by which plants maintain the subtle balance between growth and defense to avoid excessive growth or defense in response to constant biotrophic pathogen attack.
In loving memory of Professor Shiping Wang Mol. Plant (IF 10.812) Pub Date : 2019-07-31 Meng Yuan
We are deeply saddened that our respected Dr. Shiping Wang passed away on May 14, 2019 at the age of 64 after a hard-fought battle with cancer for four years and seven months. Dr. Wang was a professor of plant pathology at Huazhong Agricultural University. She was also a beloved wife, mother, mentor and friend. We shall miss her dearly.
More Transporters, More Substrates: The Arabidopsis Major Facilitator Superfamily Revisited Mol. Plant (IF 10.812) Pub Date : 2019-07-19 María Niño-González, Esther Novo-Uzal, Dale N. Richardson, Pedro M. Barros, Paula Duque
The Major Facilitator Superfamily (MFS) is ubiquitous in living organisms and represents the largest group of secondary active membrane transporters. In plants, significant research efforts have focused on the role of specific families within the MFS, particularly those transporting macronutrients (C, N and P) that comprise the vast majority of the members of this superfamily. Other MFS families remain less explored, though a plethora of additional substrates and physiological functions have been uncovered. Nevertheless, the lack of a systematic approach to the analysis of the MFS as a whole has obscured the high diversity and versatility of these transporters. Here, we present a phylogenetic analysis of all annotated MFS domain-containing proteins encoded in the Arabidopsis thaliana genome and propose that this superfamily of transporters consists of 218 members, clustered in 22 families. In reviewing the available information regarding the diversity in biological functions and substrates of arabidopsis MFS members, we provide arguments for intensified research on these membrane transporters to unveil the breadth of their physiological relevance, disclose the molecular mechanisms underlying their mode of action, and explore their biotechnological potential.
Nucleocytoplasmic Trafficking of the Arabidopsis WD40 Repeat Protein XIW1 Regulates ABI5 Stability and Abscisic Acid Responses Mol. Plant (IF 10.812) Pub Date : 2019-07-08 Xuezhong Xu, Wang Wan, Guobin Jiang, Yue Xi, Haijian Huang, Jiajia Cai, Yanan Chang, Cheng-Guo Duan, Satendra K. Mangrauthia, Xinxiang Peng, Jian-Kang Zhu, Guohui Zhu
WD40 repeat-containing proteins (WD40 proteins) serve as versatile scaffolds for protein-protein interactions, modulating a variety of cellular processes such as plant stress and hormone responses. Here, we describe a WD40 protein, XIW1 (for XPO1-Interacting WD40 protein 1), that positively regulates the Abscisic acid (ABA) response in Arabidopsis. XIW1 is located in the cytoplasm and nucleus. It interacts with the nuclear transport receptor XPO1 and is exported by XPO1 from the nucleus. Mutation of XIW1 reduces the induction of ABA-responsive genes and the accumulation of ABA Insensitive 5 (ABI5), leading to ABA-insensitive phenotypes during seed germination and seedling growth, and decreased drought stress resistance. ABA treatment upregulates the expression of XIW1, and both ABA and abiotic stresses promote the nuclear accumulation of the XIW1 protein. In the nucleus, XIW1 interacts with ABI5, and loss of XIW1 results in rapid proteasomal degradation of ABI5. Taken together, these data suggest that XIW1 is a nucleocytoplasmic shuttling protein that has a positive role in ABA responses by interacting with and maintaining the stability of ABI5 in the nucleus.
GTR-mediated radial import directs accumulation of defensive glucosinolates to sulfur-rich cells (S-cells) in phloem cap of inflorescence stem of Arabidopsis thaliana Mol. Plant (IF 10.812) Pub Date : 2019-06-29 Deyang Xu, Pascal Hunziker, Olga Koroleva, Andreas Blennow, Christoph Crocoll, Alexander Schulz, Hussam Hassan Nour-Eldin, Barbara Ann Halkier
In the phloem cap region of Arabidopsis, sulfur-rich cells (S-cells) accumulate >100 mM glucosinolates (GLS), but are biosynthetically inactive. The source and route of S-cell-bound GLS remain elusive. Here we used single-cell sampling and scanning electron microscopy with Energy-dispersive X-ray analysis to show that the GLS importers NPF2.10/GTR1 and NPF2.11/GTR2 are critical for GLS accumulation in S-cells, although not localized to the S-cells. Analysis of S-cell GLS in homo- and heterografts of gtr1 gtr2, and biosynthetic null mutant on wild type indicate that S-cells accumulate GLS via symplasmic connections either directly from neighboring biosynthetic cells or indirectly to non-neighboring cells expressing GTRs. Distinct sources and transport routes exist for different types of GLS, and vary dependent on the position of S-cells in the inflorescence stem. Based on our data, we propose a model for GLS transport routes either directly from biosynthetic cells or via GTR-mediated import from apoplastic space radially into a symplasmic domain wherein the S-cells are the ultimate sink. Similarly, we observed accumulation of the cyanogenic glucoside defense compounds in high-turgor cells in phloem cap of Lotus japonicus, suggesting that storage of defense compounds in high-turgor cells may be a general mechanism for chemical protection of the phloem cap.
Perspectives on the application of genome editing technologies in crop breeding Mol. Plant (IF 10.812) Pub Date : 2019-06-28 Kai Hua, Jinshan Zhang, Jose Ramon Botella, Changle Ma, Fanjiang Kong, Baohui Liu, Jian-Kang Zhu
Most conventional and modern crop improvement methods exploit natural or artificially induced genetic variations and require laborious characterization of multiple generations of time-consuming genetic crosses. Genome editing systems, in contrast, provide the means to rapidly modify genomes in a precise and predictable way, making it possible to introduce improvements directly into elite varieties. Here, we describe the range of applications available to agricultural researchers using existing genome editing tools. In addition to providing examples of genome editing applications in crop breeding, we discuss the technical and social challenges faced by breeders using genome editing tools for crop improvement.
BZR1 Family Transcription Factors Function Redundantly and Indispensably in BR Signaling but Exhibit BRI1-Independent Function in Regulating Anther Development in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-06-21 Lian-Ge Chen, Zhihua Gao, Zhiying Zhao, Xinye Liu, Yongpeng Li, Yuxiang Zhang, Xigang Liu, Yu Sun, Wenqiang Tang
BRASSINAZOLE RESISTANT 1 family proteins (BZRs) are central transcription factors that govern brassinosteroid (BR)-regulated gene expression and plant growth. However, it is unclear whether there exists a BZRs-independent pathway that mediates BR signaling. In this study, we found that knocking out the expression of all BZRs in Arabidopsis generated a hextuple mutant (bzr-h) displays vegetative growth phenotypes that were almost identical to those of the BR receptors null mutant bri1brl1brl3 (bri-t). By RNA sequencing, we found that global gene expression in bzr-h was unaffected by 2 h of BR treatment. The anthers of bzr-h plants were loculeless, but a similar phenotype was not observed in bri-t, suggesting that BZRs have a BR signaling-independent regulatory role in anther development. By real-time PCR and in situ hybridization, we found that the expression of SPOROCYTELESS (SPL), a transcription factor gene that is essential for anther locule development, was barely detectable in the bzr-h mutant, suggesting that BZRs regulate locule development by regulating SPL expression. Together, our findings not only demonstrate that BZRs are indispensable transcription factors for the regulation of both BR signaling and anther locule development, but also provide new insight into the molecular mechanisms that control microsporogenesis process in Arabidopsis.
Elimination of a retrotransposon for quenching genome instability in modern rice Mol. Plant (IF 10.812) Pub Date : 2019-06-20 Yu Peng, Yingying Zhang, Yijie Gui, Dong An, Junzhong Liu, Xun Xu, Qun Li, Junmin Wang, Wen Wang, Chunhai Shi, Longjiang Fan, Baorong Lu, Yiwen Deng, Sheng Teng, Zuhua He
Transposable elements (TEs) constitute the most abundant portions of plant genomes and can dramatically shape host genomes during plant evolution. They also play important roles in crop domestication. However, whether TEs themselves are also selected during crop domestication remained unknown. Here, we identify an active long terminal repeat (LTR) retrotransposon, HUO, as a potential selection target during rice domestication and breeding. HUO is a low-copy-number LTR retrotransposon, and displays transposition activity under the natural growth conditions and transmits transpositions through male gametogenesis, preferentially inserting into genomic regions capable of transcription. HUO exists in all wild rice accessions, about half of the archaeological rice grains (1200-7000 years ago) and landraces, but is absent in almost all modern varieties, indicating its gradual elimination during rice domestication and breeding. Our data hints that HUO is subjected to strict gene silencing through the RNA-directed DNA methylation (RdDM) pathway. Our study also suggests that HUO may trigger genomic defense through altering genome-wide DNA methylation and small RNA biogenesis, and changing global gene expression, resulting in decreased disease resistance and yield, which may explain its elimination in rice breeding. Thus, our study reveals that negative selection of an active retrotransposon may be important for genome stability during crop domestication and breeding.
Whole-plant live imaging of reactive oxygen species Mol. Plant (IF 10.812) Pub Date : 2019-06-18 Yosef Fichman, Gad Miller, Ron Mittler
Reactive oxygen species (ROS) are key regulators of numerous subcellular, cellular and systemic signals. They function in plants as an integral part of many different hormonal, physiological and developmental pathways, as well as play a critical role in defense and acclimation responses to different biotic and abiotic conditions. Although many ROS imaging techniques have been developed and utilized in plants, a whole-plant imaging platform for the dynamic detection of ROS in mature plants is lacking. Here we describe a robust and straightforward method for the whole-plant live imaging of ROS in mature plants grown in soil. The new method could be used to study local and systemic ROS signals in different genetic variants, conduct phenotyping studies to identify new pathways for ROS signaling, monitor the stress level of different plants and mutants, and unravel novel routes of ROS integration into stress, growth regulation and development in plants. We demonstrate the utility of the new method for the study of systemic ROS signals in different mutants of Arabidopsis thaliana, as well as for the study of wound responses in wheat and corn.
A GmNINa-miR172c-NNC1 Regulatory Network Coordinates the Nodulation and Autoregulation of Nodulation Pathways in Soybean Mol. Plant (IF 10.812) Pub Date : 2019-06-13 Lixiang Wang, Zhengxi Sun, Chao Su, Yongliang Wang, Qiqi Yan, Jiahuan Chen, Thomas Ott, Xia Li
Symbiotic root nodules are root lateral organs of plants in which nitrogen-fixing bacteria (rhizobia) convert atmospheric nitrogen to ammonia. The formation and number of nodules in legumes are precisely controlled by a rhizobia-induced signal cascade and host-controlled autoregulation of nodulation (AON). However, how these pathways are integrated and their underlying mechanisms are unclear. Here, we report that the microRNA172c (miR172c) activates soybean (Glycine max) Rhizobia-Induced CLE1 (GmRIC1) and GmRIC2 by removing the transcriptional repression of these genes by soybean Nodule Number Control 1 (NNC1), thereby activating the AON pathway. NNC1 interacts with GmNINa, the soybean ortholog of Lotus NODULE INCEPTION (NIN) and hampers its transcriptional activation of GmRIC1 and GmRIC2. Importantly, GmNINa acts as a transcriptional activator of miR172c. Intriguingly, NNC1 can transcriptionally repress miR172c expression, introducing a novel negative feedback loop into the NNC1 regulatory network. Moreover, GmNINa interacts with NNC1 and can relieve the NNC1-mediated repression of miR172c transcription. Thus, the GmNINa/miR172c/NNC1 network is a master switch that coordinately regulates and optimizes NF and AON signaling, supporting the balance between nodulation and AON in soybean.
OsBRXL4 Regulates Shoot Gravitropism and Rice Tiller Angle through Affecting LAZY1 Nuclear Localization Mol. Plant (IF 10.812) Pub Date : 2019-06-12 Zhen Li, Yan Liang, Yundong Yuan, Lei Wang, Xiangbing Meng, Guosheng Xiong, Jie Zhou, Yueyue Cai, Ningpei Han, Lekai Hua, Guifu Liu, Jiayang Li, Yonghong Wang
Rice tiller angle is a key agronomic trait that contributes to ideal plant architecture and grain production. Our previous study showed that LAZY1 (LA1) controls tiller angle via affecting shoot gravitropism, but the molecular mechanism remains largely unknown. Here, we identified a LA1-interacting protein named Brevis Radix Like 4 (OsBRXL4). We showed that the interaction between OsBRXL4 and LA1 occurs at the plasma membrane and that their interaction determines LA1 nuclear localization. We found that LA1 nuclear localization is essential for LA1 function, which is different from AtLA1, the ortholog in Arabidopsis. Overexpression of OsBRXL4 leads to a prostrate growth phenotype, whereas OsBRXLs RNAi plants, in which the expression levels of OsBRXL1, OsBRXL4, and OsBRXL5 were decreased, display a compact phenotype. Further genetic evidence confirmed that OsBRXL4 controls rice tiller angle by affecting LA1 nuclear localization. Consistent with this, OsBRXL4 regulates the shoot gravitropism through affecting polar auxin transport as did LA1. Therefore, our study not only identifies OsBRXL4 as a regulatory component of rice tiller angle, but also provides a new insight into our understanding of rice plant architecture.
The Structure and Function of Major Plant Metabolite Modifications Mol. Plant (IF 10.812) Pub Date : 2019-06-11 Shouchuang Wang, Saleh Alseekh, Alisdair R. Fernie, Jie Luo
Plants produce myriad structurally and functionally diverse metabolites that play many different roles in growth and development and in response to continually changing environmental conditions and abiotic and biotic stresses. This metabolic diversity is, to a large extent, due to chemical modification of the basic skeletons of metabolites. Here, we review the major known plant metabolite modifications and summarize the progress and challenges that have been achieved in the field. We cover both technical and functional aspects focusing on the influence that various modifications have on biosynthesis, degradation, transport, and storage of metabolites, as well as their bioactivity and toxicity. Finally, emerging insight into the evolution of metabolic pathways and metabolite functionality will be described.
Wxlv, the ancestral allele of rice Waxy gene Mol. Plant (IF 10.812) Pub Date : 2019-06-08 Changquan Zhang, Jihui Zhu, Shengjie Chen, Xiaolei Fan, Qianfeng Li, Yan Lu, Min Wang, Hengxiu Yu, Chuandeng Yi, Shuzhu Tang, Minghong Gu, Qiaoquan Liu
In rice grains, the Waxy (Wx) gene is responsible for the synthesis of amylose, the most important determinant for eating and cooking quality. Up to now, several Wx alleles have been elucidated on their effects of amylose content as well as the taste of cooked rice. However, the relationships between artificial selection and the evolution as well as distribution of various Wx alleles remain unclear. Herein, we report the cloning of the ancestral allele Wxlv of the Wx locus, which dramatically affects the mouthfeel of rice grains by modulating the size of amylose molecules. We demonstrated that Wxlv originated directly from wild rice, and the three major Wx alleles in cultivated rice (Wxb, Wxa, and Wxin) differentiated after the substitution of one base pair at the functional sites. These data indicate that the Wxlv allele played an important role in artificial selection and domestication. The findings also shed light on the evolution of various Wx alleles, which have greatly contributed to improving the eating and cooking quality of rice.
Wound-induced shoot-to-root relocation of JA-Ile precursors coordinates Arabidopsis growth Mol. Plant (IF 10.812) Pub Date : 2019-06-08 Adina Schulze, Marlene Zimmer, Stefan Mielke, Hagen Stellmach, Charles W. Melnyk, Bettina Hause, Debora Gasperini
Multicellular organisms rely upon the movement of signaling molecules across cells, tissues and organs to communicate among distal sites. In plants, localized leaf damage activates jasmonate (JA)-dependent transcriptional reprogramming in both harmed and unharmed tissues. Although previous evidence indicated that JA species can translocate from damaged into distal sites, the identity of the mobile compound(s), the tissues through which they translocate and the impact of their relocation remain unknown. Here, we found that following shoot wounding, the relocation of endogenous jasmonates through the phloem is essential to initiate JA signaling and stunt growth in unharmed roots of Arabidopsis thaliana. By coupling grafting experiments to hormone profiling, we uncovered that the hormone precursor OPDA and its derivatives, but not the bioactive JA-Ile conjugate, translocate from wounded shoots into undamaged roots. Upon root relocation, the mobile precursors cooperatively regulated JA responses through their conversion into JA-Ile and JA signaling activation. Collectively, our findings demonstrate the existence of long-distance translocation of endogenous OPDA and its derivatives which serve as communication molecules to coordinate shoot-to-root responses, and highlight the importance of a controlled re-distribution of hormone precursors among organs during plant stress acclimation.
ETR1 Integrates Response to Ethylene and Cytokinins into a Single Multistep Phosphorelay Pathway to Control Root Growth Mol. Plant (IF 10.812) Pub Date : 2019-06-07 Marketa Zdarska, Abigail Rubiato Cuyacot, Paul T. Tarr, Amel Yamoune, Agnieszka Szmitkowska, Vendula Hrdinová, Zuzana Gelová, Elliot M. Meyerowitz, Jan Hejátko
Cytokinins and ethylene control plant development via sensors from the histidine kinase (HK) family. However, downstream signaling pathways for the key phytohormones are distinct. Here we report not only cytokinin but also ethylene is able to control root apical meristem (RAM) size through activation of the multistep phosphorelay (MSP) pathway. We find both cytokinin and ethylene-dependent RAM shortening requires ethylene binding to ETR1 and its HK activity. The receiver domain of ETR1 interacts with MSP signaling intermediates acting downstream of cytokinin receptors, further substantiating the role of ETR1 in MSP signaling. Our studies find both cytokinin and ethylene induce the MSP in similar and distinct cell types with ETR1-mediated ethylene signaling controlling MSP output specifically in the root transition zone. We identified members of the MSP pathway specific and common to both hormones and show that ETR1-regulated ARR3 controls RAM size. ETR1-mediated MSP spatially differs from canonical CTR1/EIN2/EIN3 ethylene signaling and is independent of EIN2, indicating that both pathways can be spatially and functionally separated. Furthermore, we demonstrate that canonical ethylene signaling controls MSP responsiveness to cytokinin specifically in the root transition zone, presumably via regulation of ARR10, one of the positive regulators of MSP signaling in Arabidopsis.
A Post-domestication Mutation Dt2 Triggers Systemic Modification of Divergent and Convergent Pathways Modulating Multiple Agronomic Traits in Soybean Mol. Plant (IF 10.812) Pub Date : 2019-05-29 Dajian Zhang, Xutong Wang, Shuo Li, Chaofan Wang, Michael J. Gosney, Michael V. Mickelbart, Jianxin Ma
The semi-determinate stem growth habit in leguminous crops, similar to the “green revolution” semi-dwarf trait in cereals, is a key plant architecture trait that affects several other traits determining grain yield. In soybean, semi-determinacy is modulated by a post-domestication gain-of-function mutation, Dt2, that encodes a MADS-domain transcription factor. However, its role in systemic modification of stem growth and other traits is unknown. Here, we show that Dt2 functions not only as a direct repressor of Dt1 that prevents terminal flowering, but also as a direct activator of putative floral integrator/identity genes including GmSOC1, GmAP1, and GmFUL that may promote flowering. We also demonstrate that Dt2 functions as a direct repressor of putative drought responsive transcription factor gene GmDREB1D, and as a direct activator of GmSPCH and GmGRP7 that are potentially associated with asymmetric young epidermal cell division and stomatal opening, respectively, which may affect the plant’s water-use efficiency (WUE). More intriguingly, Dt2 was found to be a direct activator or repressor of the precursors of eight miRNAs targeting genes potentially associated with meristem maintenance, flowering time, stomatal density, WUE, and/or stress responses. This study, thus, reveals the molecular basis of pleiotropy associated with plant productivity, adaptability, and environmental resilience.
Phosphorylation of LTF1, A MYB Transcription Factor in Populus, Acts as a Sensory Switch Regulating Lignin Biosynthesis in Wood Cells Mol. Plant (IF 10.812) Pub Date : 2019-05-27 Jinshan Gui, Laifu Luo, Yu Zhong, Jiayan Sun, Toshiaki Umezawa, Laigeng Li
Lignin is specifically deposited in plant secondary cell walls and initiation of lignin biosynthesis is regulated by a variety of developmental and environmental signals. However, the mechanism governing the regulation of lignin biosynthesis remains to be elucidated. Here, we identified a lignin biosynthesis associated transcription factor (LTF) from Populus, LTF1, which binds to the promoter of 4-coumarate-CoA ligase (4CL), a key lignin biosynthetic gene. We showed that LTF1 in its unphosphorylated state functions as a regulator to restrain lignin biosynthesis. When LTF1 becomes phosphorylated by PdMPK6 in response to external stimuli such as wounding, it underwent degradation through a proteasome pathway, resulting in activation of lignification. Expression of the LTF1 phosphorylation-null mutation led to stable LTF1 accumulation and persistent attenuation of lignification in wood cells. The study reveals a mechanism where LTF1 phosphorylation acts as a sensory switch to regulate lignin biosynthesis in response to environmental stimuli. The discovery of novel modulators and mechanisms to modify lignin biosynthesis has important implications for improving the utilization of cell wall biomass.
Genome sequences provide insights into the reticulate origin and unique traits of woody bamboos Mol. Plant (IF 10.812) Pub Date : 2019-05-27 Zhen-Hua Guo, Peng-Fei Ma, Guo-Qian Yang, Jin-Yong Hu, Yun-Long Liu, En-Hua Xia, Mi-Cai Zhong, Lei Zhao, Gui-Ling Sun, Yu-Xing Xu, You-Jie Zhao, Yi-Chi Zhang, Yu-Xiao Zhang, Xue-Mei Zhang, Meng-Yuan Zhou, Ying Guo, Cen Guo, Jing-Xia Liu, De-Zhu Li
Polyploidization is a major driver of speciation and its importance to plant evolution has been well recognized. Bamboos comprise of one diploid herbaceous and three polyploid woody lineages, and are the only major subfamily in grasses which diversified in forests with tree-like lignified culm for its woody members. Here we generated four draft genomes of major bamboo lineages at three different ploidy levels (diploid, tetraploid and hexaploid). We also constructed a high-density genetic linkage map of bamboo for a hexaploid species, providing a linkage-map-based strategy for assembly and identification of subgenomes in polyploids. Further phylogenomic analyses based on a large dataset of syntenic genes with expected copies revealed that woody bamboos originated subsequent to the divergence of the herbaceous bamboo lineage, and experienced complex reticulate evolution by three independent allopolyploid events involving four extinct diploid ancestors. A shared but distinct subgenome was identified in all polyploid forms, and its progenitor could be critical in ancient polyploidizations and origin of woody bamboos. We also found important genetic clues to the unique flowering behavior and woody trait in bamboos. Taken together, our study provides significant insights into ancient reticulate evolution at the subgenome level in the absence of extant donor species, and offers a potential model scenario for a broad-scale study of plant origins by allopolyploidization in angiosperms.
Systems biology of plant microbiome interactions Mol. Plant (IF 10.812) Pub Date : 2019-05-23 Patricia A. Rodriguez, Michael Rothballer, Soumitra Paul Chowdhury, Thomas Nussbaumer, Caroline Gutjahr, Pascal Falter-Braun
In natural environments plants are exposed to diverse microbiota that they interact with in complex ways. While plant-pathogen interactions have been intensely studied to understand defense mechanisms in plants, many microbes and microbial communities can have substantial beneficial effects on their plant host. Such beneficial effects include improved acquisition of nutrients, accelerated growth, resilience against pathogens, and improved resistance against abiotic stress conditions such as heat, drought, and salinity. However, the beneficial effects of bacterial strains or consortia on their host are often cultivar- and species-specific posing an obstacle to their general application. Remarkably many of the signals that trigger plant immune responses are molecularly highly similar and often identical in pathogenic and beneficial microbes. Thus, it is unclear what determines the outcome of a particular microbe-host interaction and which factors enable plants to distinguish beneficials from pathogens. To unravel the complex network of genetic, microbial, and metabolic interactions including the signaling events mediating microbe-host interactions, comprehensive quantitative systems biology approaches will be needed.
Systems biology approach pinpoints minimum requirements for auxin distribution during fruit opening Mol. Plant (IF 10.812) Pub Date : 2019-05-23 Xin-Ran Li, Renske M.A. Vroomans, Samantha Fox, Verônica A. Grieneisen, Lars Østergaard, Athanasius F.M. Marée
The phytohormone auxin is implied in steering various developmental decisions during plant morphogenesis in a concentration-dependent manner. Auxin maxima have been shown to maintain meristematic activity, for example of the root apical meristem, and position new sites of outgrowth, such as during lateral root initiation and phyllotaxis. More recently, it has been demonstrated that sites of auxin minima also provide positional information. In the developing Arabidopsis fruit, auxin minima are required for correct differentiation of the valve margin. It remains unclear, however, how this auxin minimum is generated and maintained. Here we employ a systems biology approach to model auxin transport based on experimental observations. This allows us to determine the minimal requirements for its establishment. Our simulations reveal that two alternative processes — which we coin “flux-barrier” and “flux-passage” — are both able to generate an auxin minimum, but under different parameter settings. Both models are in principle able to yield similar auxin profiles but present qualitatively distinct patterns of auxin flux. The models were tested by tissue-specific inducible ablation, revealing that the auxin minimum in the fruit is most likely generated by a flux-passage process. Model predictions were further supported through 3D PIN-localisation imaging and implementing experimentally observed transporter localisation. Through such an experimental-modelling cycle, we predict how the auxin minimum gradually matures during fruit development to ensure timely fruit opening and seed dispersal.
mTERF5 Acts as a Transcriptional Pausing Factor to Positively Regulate Transcription of Chloroplast psbEFLJ Mol. Plant (IF 10.812) Pub Date : 2019-05-22 Shunhua Ding, Yi Zhang, Zhi Hu, Xiahe Huang, Bohan Zhang, Qingtao Lu, Xiaogang Wen, Yingchun Wang, Congming Lu
RNA polymerase transcriptional pausing represents a major checkpoint in transcription in bacteria and metazoans, but it is unknown whether this phenomenon occurs in plant organelles. Here, we report that transcriptional pausing occurs in chloroplasts. We found that mTERF5 specifically and positively regulates the transcription of chloroplast psbEFLJ (encoding four key subunits of photosystem II) in Arabidopsis thaliana. mTERF5 causes the plastid-encoded RNA polymerase (PEP) complex to pause at psbEFLJ by binding to the +30 to +51 position of double-stranded DNA. Moreover, mTERF5 interacts with pTAC6, an essential subunit of the PEP complex, although pTAC6 is not involved in the transcriptional pausing at psbEFLJ. mTERF5 recruits additional pTAC6 to the transcriptionally paused region of psbEFLJ and this recruited pTAC6 can be assembled into the PEP complex to regulate psbEFLJ transcription. Our findings shed light on the role of transcriptional pausing in chloroplast transcription in plants.
De Novo Domestication: An Alternative Route toward New Crops for the Future Mol. Plant (IF 10.812) Pub Date : 2019-04-15 Alisdair R. Fernie, Jianbing Yan
Current global agricultural production must feed over 7 billion people. However, productivity varies greatly across the globe and is under threat from both increased competitions for land and climate change and associated environmental deterioration. Moreover, the increase in human population size and dietary changes are putting an ever greater burden on agriculture. The majority of this burden is met by the cultivation of a very small number of species, largely in locations that differ from their origin of domestication. Recent technological advances have raised the possibility of de novo domestication of wild plants as a viable solution for designing ideal crops while maintaining food security and a more sustainable low-input agriculture. Here we discuss how the discovery of multiple key domestication genes alongside the development of technologies for accurate manipulation of several target genes simultaneously renders de novo domestication a route toward crops for the future.
Population Genomic Analysis and De Novo Assembly Reveal the Origin of Weedy Rice as an Evolutionary Game Mol. Plant (IF 10.812) Pub Date : 2019-01-30 Jian Sun, Dianrong Ma, Liang Tang, Minghui Zhao, Guangchen Zhang, Wenjia Wang, Jiayu Song, Xiang Li, Zimeng Liu, Wenxing Zhang, Quan Xu, Yuncheng Zhou, Jianzhong Wu, Toshio Yamamoto, Fei Dai, Yan Lei, Song Li, Gang Zhou, Wenfu Chen
Crop weediness, especially that of weedy rice (Oryza sativa f. spontanea), remains mysterious. Weedy rice possesses robust ecological adaptability; however, how this strain originated and gradually formed proprietary genetic features remains unclear. Here, we demonstrate that weedy rice at Asian high latitudes (WRAH) is phylogenetically well defined and possesses unselected genomic characteristics in many divergence regions between weedy and cultivated rice. We also identified novel quantitative trait loci underlying weedy-specific traits, and revealed that a genome block on the end of chromosome 1 is associated with rice weediness. To identify the genomic modifications underlying weedy rice evolution, we generated the first de novo assembly of a high-quality weedy rice genome (WR04-6), and conducted a comparative genomics study between WR04-6 with other rice reference genomes. Multiple lines of evidence, including the results of demographic scenario comparisons, suggest that differentiation between weedy rice and cultivated rice was initiated by genetic improvement of cultivated rice and that the essence of weediness arose through semi-domestication. A plant height model further implied that the origin of WRAH can be modeled as an evolutionary game and indicated that strategy-based selection driven by fitness shaped its genomic diversity.
A Single-Cell RNA Sequencing Profiles the Developmental Landscape of Arabidopsis Root Mol. Plant (IF 10.812) Pub Date : 2019-04-17 Tian-Qi Zhang, Zhou-Geng Xu, Guan-Dong Shang, Jia-Wei Wang
Cells of eukaryotic multicellular organisms have inherent heterogeneity. Recent advances in single-cell gene expression studies enable us to explore transcriptional regulation in dynamic development processes and highly heterogeneous cell populations. In this study, using a high-throughput single-cell RNA-sequencing assay, we found that the cells in Arabidopsis root are highly heterogeneous in their transcriptomes. A total of 24 putative cell clusters and the cluster-specific marker genes were identified. The spatial distribution and temporal ordering of the individual cells at different developmental stages illustrate their hierarchical structures and enable the reconstruction of continuous differentiation trajectory of root development. Moreover, we found that each root cell cluster exhibits distinct patterns of ion assimilation and hormonal responses. Collectively, our study reveals a high degree of heterogeneity of root cells and identifies the expression signatures of intermediate states during root cell differentiation at single-cell resolution. We also established a web server (http://wanglab.sippe.ac.cn/rootatlas/) to facilitate the use of the datasets generated in this study.
Lower Temperature 1 Enhances Aba Responses And Plant Drought Tolerance By Modulating The Stability And Localization Of C2-Domain Aba-Related Proteins In Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-05-16 Tao Qin, Qiuzhen Tian, Guifeng Wang, Liming Xiong
Plasma membrane associated abscisic acid (ABA) signal transduction is an integral part of ABA signaling. The C2-domain ABA-related (CAR) proteins play important roles in the recruitment of ABA receptors to the plasma membrane to facilitate ABA signaling yet how CAR proteins are regulated is unclear. In this study, we conducted a genetic screen for leaf transpiration mutants and identified an uncharacterized protein, LOT1 (LOWER TEMPERATURE 1), that regulates the dynamic localization and stability of CAR proteins. The lot1 mutant had a lower leaf temperature relative to the wild type due to higher transpiration. We found that LOT1 interacts with CAR9 in yeast and in planta. ABA reduces LOT1-CAR9 interaction in the nucleus likely via Ca2+, which results in increased distribution of CAR9 to the plasma membrane. We further found that the stability of CAR9 is affected by LOT1. Less CAR9 protein was accumulated and more was ubiquitinated in lot1. While lot1, car9 and lot1 car9 double mutant were hyposensitive to ABA, the hyposensitive phenotype of lot1 could be rescued by overexpressing CAR9. Our study characterized a new protein that regulates plant tolerance to drought stress by affecting ABA signaling through regulating the stability and dynamic localization of CAR9.
Natural Variation in CCD4 Promoter Underpins Species-specific Evolution of Red Coloration in Citrus Peel Mol. Plant (IF 10.812) Pub Date : 2019-05-16 Xiongjie Zheng, Kaijie Zhu, Quan Sun, Weiyi Zhang, Xia Wang, Hongbo Cao, Meilian Tan, Zongzhou Xie, Yunliu Zeng, Junli Ye, Lijun Chai, Qiang Xu, Zhiyong Pan, Shunyuan Xiao, Paul D. Fraser, Xiuxin Deng
Carotenoids and apocarotenoids can act as phytohormones and volatile precursors that influence plant development and confer aesthetic and nutritional value critical to consumer preference. Citrus fruits display considerable natural variation for carotenoid and apocarotenoid pigments. A multifaceted genetic approach revealed that a 5´cis-regulatory change at CCD4b encoding CAROTENOID CLEAVAGE DIOXYGENASE 4b is a major genetic determinant for the natural variation of C30 apocarotenoids responsible for the red coloration of citrus peel. Functional analyses demonstrated that besides its known role in synthesizing β-citraurin, CCD4b is also responsible for the production of another important C30 apocarotenoid pigment, β-citraurinene. Furthermore, promoter and transcript analyses for CCD4b among citrus germplasm accessions established a tight correlation between presence of a putative 5´ cis-regulatory enhancer within a MITE transposon and the enhanced allelic expression of CCD4b in C30 apocarotenoid-rich red-peeled accessions. A phylogenetic analysis provides evidence that functional diversification and naturally occurring promoter variation of CCD4b constituted the stepwise evolution of red peels in mandarins and their hybrids. Our findings provide insight into the genetic and evolutionary basis of apocarotenoid diversity in plants and may also facilitate breeding efforts that aim to improve the nutritional and aesthetic value of citrus and perhaps other fruit crops.
Maize Carbohydrate partitioning defective33 encodes a MCTP protein and functions in sucrose export from leaves Mol. Plant (IF 10.812) Pub Date : 2019-05-16 Thu M. Tran, Tyler J. McCubbin, Saadia Bihmidine, Benjamin T. Julius, R. Frank Baker, Martin Schauflinger, Clifford Weil, Nathan Springer, Paul Chomet, Ruth Wagner, Jeff Woessner, Karen Grote, Jeanette Peevers, Thomas L. Slewinski, David M. Braun
To sustain plant growth, development, and crop yield, sucrose must be transported from leaves to distant parts of the plant, such as seeds and roots. To identify genes that regulate sucrose accumulation and transport in maize (Zea mays), we isolated carbohydrate partitioning defective33 (cpd33), a recessive mutant that accumulated excess starch and soluble sugars in mature leaves. The cpd33 mutants also exhibited chlorosis in the leaf blades, greatly diminished plant growth, and reduced fertility. Cpd33 encodes a protein containing multiple C2 domains and transmembrane regions. Subcellular localization experiments showed the CPD33 protein localized to plasmodesmata (PD), the plasma membrane, and the endoplasmic reticulum. We also found that a loss-of-function-mutant of the CPD33 homolog in Arabidopsis, QUIRKY, had a similar carbohydrate hyperaccumulation phenotype. Radioactively labeled sucrose transport assays showed that sucrose export was significantly lower in cpd33 mutant leaves relative to wild-type leaves. However, PD transport in the adaxial-abaxial direction was unaffected in cpd33 mutant leaves. Intriguingly, transmission electron microscopy revealed fewer PD at the companion cell – sieve element interface in mutant phloem tissue, providing a possible explanation for the reduced sucrose export in mutant leaves. Collectively, our results suggest that CPD33 functions to promote symplastic transport into sieve elements.
Folate Metabolism Interferes Plant Immunity through 1C Methionine Synthase-directed Genome-wide DNA Methylation Enhancement Mol. Plant (IF 10.812) Pub Date : 2019-05-09 Beatriz González, Pablo Vera
Plants rely on primary metabolism for flexible adaptation to environmental changes. Here, through a combination of chemical genetics and forward genetic studies in Arabidopsis plants we identified that the essential folate metabolic pathway exerts a salicylic acid (SA)-independent negative control on plant immunity. Disruption of the folate pathway promotes enhanced resistance to Pseudomonas syringae DC3000 via activation of a primed immune state in the plant, and its implementation results in enhanced susceptibility. Comparative proteomics analysis using immune-defective mutants identified a methionine synthase (METS1), in charge of the synthesis of Met through the folate-dependent 1C metabolism, acting as a nexus between the folate pathway and plant immunity. Overexpression of METS1 represses plant immunity and is accompanied by genome-wide global increase in DNA methylation, revealing that imposing a methylation pressure at the genome level compromises plant immunity. These observations therefore provide evidences indicating that the folate pathway represents a new layer of complexity in the regulation of plant defense responses.
Translational Regulation of Plant Response to High Temperature by a Dual Function tRNAHis Guanylyltransferase in Rice Mol. Plant (IF 10.812) Pub Date : 2019-05-07 Ke Chen, Tao Guo, Xin-Min Li, Yi-Min Zhang, Yi-Bing Yang, Wang-Wei Ye, Nai-Qian Dong, Chuan-Lin Shi, Yi Kan, You-Huang Xiang, Hai Zhang, Ya-Chao Li, Ji-Ping Gao, Xuehui Huang, Qiang Zhao, Bin Han, Jun-Xiang Shan, Hong-Xuan Lin
Plants are sessile organisms, and have thus evolved numerous strategies to acclimate to changes in environmental temperature. There is emerging evidence to describe the molecular basis of this acclimation. In this study, we identified a tRNAHis guanylyltransferase, AET1, that contributes to the modification of pre-tRNAHis and is required for normal growth under high temperature conditions in rice. Interestingly, AET1 possibly interacts with both RACK1A and eIF3h in the ER (endoplasmic reticulum). Notably, AET1 can directly bind to the OsARF mRNAs including the uORFs of OsARF19 and OsARF23, indicating that AET1 is associated with translation regulation. Furthermore, polysome profiling assays suggest that the translational status remains unaffected in the aet1 mutant, but that the translational efficiency of OsARF19 and OsARF23 is reduced; moreover, the OsARF23 protein levels are obviously decreased in the aet1 mutant under high temperature, implying that AET1 regulates auxin signaling in response to high temperature. Our findings provide new insights into the molecular mechanisms that AET1 plays a dual function in tRNA modification and translational control involved in the regulation of the environmental temperature response in rice.
Transcriptional regulation of miR528 by OsSPL9 orchestrates antiviral response in rice Mol. Plant (IF 10.812) Pub Date : 2019-05-03 Shengze Yao, Zhirui Yang, Rongxin Yang, Yu Huang, Ge Guo, Xiangyue Kong, Ying Lan, Tong Zhou, He Wang, Wenming Wang, Xiaofeng Cao, Jianguo Wu, Yi Li
Many microRNAs (miRNAs) are critical regulators of plant antiviral defense. However, little is known as to how these miRNAs respond to virus invasion at the transcriptional level. We established previously that defense to Rice stripe virus (RSV) invasion entailed a reduction of miR528 accumulation in rice, thus alleviating miR528-mediated degradation of L-Ascorbate Oxidase (AO) mRNA, bolstering the antiviral activity of AO. Here we show that this miR528-AO defense module is also regulated by the transcription factor SPL9. SPL9 displayed high affinity binding to specific motifs within the promoter region of miR528 and activated the transcription of miR528 promoter in vivo assay. Loss-of-function mutations in SPL9 correlated with a significant reduction of miR528 but a substantial increase of AO mRNA, enhancing rice resistance to RSV. Conversely, transgenic overexpression of SPL9 stimulated the expression of miR528, hence lowering the level of AO mRNA and compromising rice defense to RSV. Importantly, gain in RSV susceptibility did not occur when SPL9 overexpression was attempted in mir528 loss-of-function mutants, or in transgenic rice expressing a miR528-resistant AO. In conclusion, SPL9-mediated transcriptional activation of miR528 expression adds a novel layer of regulation of the miR528-AO antiviral defense.
Fine-Tuning of MiR528 Accumulation Modulates Flowering Time in Rice Mol. Plant (IF 10.812) Pub Date : 2019-05-03 Rongxin Yang, Pingchuan Li, Hailiang Mei, Dong Wang, Jing Sun, Chao Yang, Lili Hao, Shouyun Cao, Chengcai Chu, Songnian Hu, Xianwei Song, Xiaofeng Cao
In plants, microRNA (miRNA) functions in the post-transcriptional repression of target mRNAs are well-explored, but the mechanisms regulating the accumulation of miRNAs remain poorly understood. Here, we report that distinct mechanisms regulate accumulation of a monocot-specific miRNA, rice (Oryza sativa) miR528. At the transcriptional level, miR528 accumulated in older plants and exhibited diurnal rhythms; at the post-transcriptional level, aging modulated miR528 levels by enhancing pri-miR528 alternative splicing. In addition, miR528 promoted flowering under long-day conditions by targeting RED AND FAR-RED INSENSITIVE 2 (OsRFI2). Moreover, natural variation in the MIR528 promoter region caused differences in miR528 expression among rice varieties, potentially due to differences in the binding strength of the transcription factor OsSPL9. Together, our findings show evidence for fine-tuning of miR528 levels in rice and provide insight into the mechanisms that regulate MIRNA expression in plants.
SERK Receptor-Like Kinases Control Division Patterns of Vascular Precursors and Ground Tissue Stem Cells during Embryo Development in Arabidopsis Mol. Plant (IF 10.812) Pub Date : 2019-05-03 Huiqiang Li, Zeping Cai, Xiaojuan Wang, Meizhen Li, Yanwei Cui, Nan Cui, Fei Yang, Mingsong Zhu, Junxiang Zhao, Wenbin Du, Kai He, Jing Yi, Frans E. Tax, Suiwen Hou, Jia Li, Xiaoping Gou
During embryo development, the vascular precursors and the ground tissue stem cells divide to renew themselves and produce the vascular tissue, endodermal cells and cortical cells. However, the molecular mechanisms regulating division of these stem cells have remained largely elusive. In this study, we show that loss function of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) genes results in aberrant embryo development. Fewer cortical, endodermal and vascular cells are generated in the embryo of serk1 serk2 bak1 triple mutants. WUSCHEL RELATED HOMEOBOX 5 (WOX5) is ectopically expressed in vascular cells of serk1 serk2 bak1 embryos. The first transverse division of the vascular precursors in mid-globular embryos and the second asymmetric division of the ground tissue stem cells in early-heart embryos are abnormally altered to a longitudinal division. The embryo defects can be partially rescued by constitutively activated mitogen-activated protein kinase (MAPK) kinase kinase YODA (YDA) and MAPK kinase MKK5. Our results revealed that SERK-mediated signals regulate division patterns of the vascular precursors and the ground tissue stem cells likely via the YDA-MKK4/5 cascade during embryo development.
Origin and evolution of core components responsible for monitoring light environment changes during plant terrestrialization Mol. Plant (IF 10.812) Pub Date : 2019-04-19 Xue Han, Xin Chang, Zhenhua Zhang, Haodong Chen, Hang He, Bojian Zhong, Xing Wang Deng
Light serves as the source of energy as well as information signals for photosynthetic plants. During evolution, plants have acquired the ability to monitor environmental light radiation and adjust their developmental patterns to optimally utilize light energy for photosynthesis. The mechanisms of light perception and signal transduction have been comprehensively studied in the past decades, mostly in a few model plants, including Arabidopsis thaliana. However, systematic analyses of the origin and evolution of core components involved in light perception and signal transduction are still lacking. Herein, we took advantages of the recently sequenced genomes and transcriptomes covering all the main Archaeplastida clades in the public domains to identify orthologous genes of the core components involved in light perception and signal transduction and to reconstruct their evolutionary history. Our analyses suggested that the acclimation to different distributions of light quality in new environments led to the origination of specific light signaling pathways in plants. The UVR8 (UV Resistance Locus 8) signaling pathway originated during the movement of plants from the deeper sea to shallow water to deal with ultraviolet B light (UV-B). After acquisition of the UV-B adaptation, origination of the phytochrome signaling pathway helped plants to colonize the water surface where red light became the prominent light energy source. The pathway of seedling emergence, which is mediated by the combination of light and phytohormone signals to orchestrate plant growth pattern transitions, originated before the emergence of seed plants. Although cryptochromes and some key components of E3 ubiquitin ligase systems already existed before the divergence of plant and animal kingdoms, the coevolution and optimization of light perception and their downstream signal transduction components, including key transcription factors and E3 ubiquitin ligase systems, are evident during plant terrestrialization.
Tiller Bud Formation Regulators MOC3 and MOC1 Cooperatively Promote Tiller Bud Outgrowth by Activating FON1 Expression in Rice Mol. Plant (IF 10.812) Pub Date : 2019-04-29 Gaoneng Shao, Zefu Lu, Jinsong Xiong, Bing Wang, Yanhui Jing, Xiangbing Meng, Guifu Liu, Haiyan Ma, Yan Liang, Fan Chen, Yonghong Wang, Jiayang Li, Hong Yu
Tillering in rice is one of the most important agronomic traits. Rice tiller development can be divided into two main processes: the formation of the axillary bud and its subsequent outgrowth. Several genes critical for bud formation in rice have been identified by genetic studies, however, their molecular function and relationships are still largely unknown. Here, we report that MONOCULM1 (MOC1) and MONOCULM 3/TILLERS ABSENT 1/STERILE AND REDUCED TILLERING 1 (MOC3/TAB1/SRT1), two vital regulators for tiller formation in rice, could physically interact to regulate tiller bud outgrowth through upregulating the expression of FLORAL ORGAN NUMBER1 (FON1), the homolog of CLAVATA1 in rice. MOC3 could directly bind to the promoter of FON1 and subsequently activate FON1 expression. MOC1 functions as a co-activator of MOC3, which did not directly bind to the FON1 promoter, but could further activate the FON1 expression in the presence of MOC3. Accordingly, FON1 is highly expressed at axillary meristems and shows remarkable decreased expression levels in moc1 and moc3 mutants. Loss-of-function mutants of FON1 exhibit normal bud formation, but deficient bud outgrowth and reduced tiller number. Collectively, these results shed lights on the joint transcriptional regulation by MOC1 and MOC3, and establish a new framework for the control of tiller bud formation and outgrowth.
Two RING-Finger Ubiquitin E3 Ligases Regulate the Degradation of SPX4, An Internal Phosphate Sensor, for Phosphate Homeostasis and Signaling in Rice Mol. Plant (IF 10.812) Pub Date : 2019-04-17 Wenyuan Ruan, Meina Guo, Xueqing Wang, Zhenhui Guo, Zhuang Xu, Lei Xu, Hongyu Zhao, Haiji Sun, Chengqi Yan, Keke Yi
SPX-domain-containing proteins (SPXs) play an important role in inorganic phosphate (Pi) sensing, signaling, and transport in eukaryotes. In plants, SPXs are known to integrate cellular Pi status and negatively regulate the activity of Pi central regulators, the PHOSPATE STARVATION RESPONSE proteins (PHRs). The stability of SPXs, such as SPX4, is reduced under Pi-deficient conditions. However, the mechanisms by which SPXs are degraded remain unclear. In this study, using a yeast-two-hybrid screen we identified two RING-finger ubiquitin E3 ligases regulating SPX4 degradation, designated SDEL1 and SDEL2, which were post-transcriptionally induced by Pi starvation. We found that both SDELs were located in the nucleus and cytoplasm, had ubiquitin E3 ligase activity, and directly ubiquitinated the K213 and K299 lysine residues in SPX4 to regulate its stability. Furthermore, we found that PHR2, a Pi central regulator in rice, could compete with SDELs by interacting with SPX4 under Pi-sufficient conditions, which protected SPX4 from ubiquitination and degradation. Consistent with the biochemical function of SDEL1 and SDEL2, overexpression of SDEL1 or SDEL2 resulted in Pi overaccumulation and induced Pi-starvation signaling even under Pi-sufficient conditions. Conversely, their loss-of-function mutants displayed decreased Pi accumulation and reduced Pi-starvation signaling. Collectively, our study revealed that SDEL1 and SDEL2 facilitate the degradation of SPX4 to modulate PHR2 activity and regulate Pi homeostasis and Pi signaling in response to external Pi availability in rice.
Natural Variations at TIG1 Encoding a TCP Transcription Factor Contribute to Plant Architecture Domestication in Rice Mol. Plant (IF 10.812) Pub Date : 2019-04-16 Weifeng Zhang, Lubin Tan, Hongying Sun, Xinhui Zhao, Fengxia Liu, Hongwei Cai, Yongcai Fu, Xianyou Sun, Ping Gu, Zuofeng Zhu, Chuanqing Sun
The modification of plant architecture was a crucial target in rice domestication and modern genetic improvement. Although a fraction of genes regulating rice plant architecture have been characterized, the molecular mechanisms underlying rice plant architecture domestication has not been elucidated. Here we show that the phenotype of inclined growth tiller in wild rice is controlled by a single dominant gene, TILLER INCLINED GROWTH 1 (TIG1), which is on chromosome 8 and encodes a TCP transcriptional activator. The TIG1 mRNA is primarily enriched in the far-land side of tiller base, promotes cell elongation and enlarges the tiller angle in wild rice. Variations in the tig1 promoter of indica cultivars led to decreased expression of TIG1 in the far-land side of tiller base, reduced cell length and tiller angle, which led to the transition from inclined growth tiller of wild rice to the erect growth tiller during rice domestication. The TIG1 protein activates the expression of EXPA3, EXPB5 and SAUR39 to regulate cell elongation and increase the tiller angle. Selective sweep analysis revealed that the tig1 allele had been selected in indica cultivars by human beings. The cloning of TIG1 supports a new scenario of plant architecture evolution in rice.
The Reference Genome Sequence of Scutellaria baicalensis Provides Insights into the Evolution of Wogonin Biosynthesis Mol. Plant (IF 10.812) Pub Date : 2019-04-15 Qing Zhao, Jun Yang, Meng-Ying Cui, Jie Liu, Yumin Fang, Mengxiao Yan, Wenqing Qiu, Huiwen Shang, Zhicheng Xu, Reheman Yidiresi, Jing-Ke Weng, Tomáš Pluskal, Marielle Vigouroux, Burkhard Steuernagel, Yukun Wei, Lei Yang, Yonghong Hu, Xiao-Ya Chen, Cathie Martin
Scutellaria baicalensis Georgi is important in Chinese Traditional Medicine where preparations of dried roots, ‘Huang Qin’, are used for liver and lung complaints including complementary cancer treatments. We report a high-quality reference genome sequence for S. baicalensis where 93% of the 408.14 Mb genome has been assembled into 9 pseudochromosomes with a super-N50 of 33.2 Mb. Comparison of this sequence to those of closely related species in the order Lamiales, Sesamum indicum and Salvia splendens, revealed how the specialised metabolic pathway for the synthesis of 4’deoxyflavone bioactives evolved in the genus, Scutellaria. We found that the gene encoding a specific cinnamate CoA ligase likely obtained its new function following recent mutations, and four genes encoding enzymes in the 4’deoxyflavone pathway are present as tandem repeats in the genome of S. baicalensis. Further analyses revealed that gene duplications, segmental duplication, gene amplification and point mutations coupled to gene neo- and sub-functionalizations were involved in the evolution of 4’deoxyflavone synthesis in the genus, Scutellaria. The reference genome of S. baicalensis will facilitate the development of improved assemblies of genome sequences for other members of the mint family and offers an important foundation for decoding the synthetic pathways of bioactive compounds in medicinal plants. Our study not only provides significant insight into the evolution of specific flavone biosynthetic pathways in members of the mint family, Lamiaceae, but also would facilitate the development of tools for enhancing bioactive productivity by metabolic engineering in microbes or by molecular breeding in plants.
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