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New insights into the response of maize to fluctuations in the light environment

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Abstract

Light is the most important environmental cue signaling the transition from skotomorphogenesis to photomorphogenesis, thus affecting plant development and metabolic activity. How the light response mechanisms of maize seedlings respond to fluctuations in the light environment has not been well characterized to date. In this study, we built a gene coexpression network from a dynamic transcriptomic map of maize seedlings exposed to different light environments. Coexpression analysis identified ten modules and multiple genes that closely correlate with photosynthesis and characterized hub genes associated with regulatory networks, duplication events, domestication and improvement. In addition, we identified that 38% of hub genes underwent duplication events, 74% of which are related to photosynthesis. Moreover, we captured the dynamic expression atlas of gene sets involved in the chloroplast photosynthetic apparatus and photosynthetic carbon assimilation in different light environments, which should help to elucidate the key mechanisms and regulatory networks that underlie photosynthesis in maize. Insights from this study provide a valuable resource to better understand the genetic mechanisms of the response to fluctuations in the light environment in maize.

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Data availability

Sequence data from this article can be found in the National Center for Biotechnology Information Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) under accession number SRP118761.

References

  • Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X, Harberd NP (2007) DELLAs contribute to plant photomorphogenesis. Plant Physiol 143:1163–1172

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allen JF (2002) Photosynthesis of ATP—electrons, proton pumps, rotors, and poise. Cell 110:273–276

    CAS  PubMed  Google Scholar 

  • Alter P, Dreissen A, Luo FL, Matsubara S (2012) Acclimatory responses of Arabidopsis to fluctuating light environment: comparison of different sunfleck regimes and accessions. Photosynth Res 113:221–237

    CAS  PubMed  PubMed Central  Google Scholar 

  • Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M (2008) Computing topological parameters of biological networks. Bioinformatics 24:282–284

    CAS  PubMed  Google Scholar 

  • Ballesteros ML, Bolle C, Lois LM, Moore JM, Vielle-Calzada JP, Grossniklaus U, Chua NH (2001) LAF1, a MYB transcription activator for phytochrome A signaling. Genes Dev 15:2613–2625

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baumgardt RL, Oliverio KA, Casal JJ, Hoecker U (2002) SPA1, a component of phytochrome A signal transduction, regulates the light signaling current. Planta 215:745–753

    CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 57:289–300

    Google Scholar 

  • Boeckx T, Winters AL, Webb KJ, Kingston-Smith AH (2015) Polyphenol oxidase in leaves: is there any significance to the chloroplastic localization? J Exp Bot 66:3571–3579

    CAS  PubMed  Google Scholar 

  • Brohammer AB, Kono TJY, Springer NM, McGaugh SE, Hirsch CN (2018) The limited role of differential fractionation in genome content variation and function in maize (Zea mays L.) inbred lines. Plant J 93:131–141

    CAS  PubMed  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    CAS  PubMed  Google Scholar 

  • Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10:673–683

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cockburn W (1983) C3 C4: Mechanisms, and cellular and environmental regulation, of photosynthesis (Book). Plant Cell Environ 6:747–748

    Google Scholar 

  • Darko E, Heydarizadeh P, Schoefs B, Sabzalian MR (2014) Photosynthesis under artificial light: the shift in primary and secondary metabolism. Philos Trans R Soc Lond B Biol Sci 369:20130243

    PubMed  PubMed Central  Google Scholar 

  • de Wit M, Galvao VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:513–537

    PubMed  Google Scholar 

  • Deng X-W, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71:791–801

    CAS  PubMed  Google Scholar 

  • Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1994) Light inactivation of arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its ucleocytoplasmic partitioning. Cell 79:1035–1045

    PubMed  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64-70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    CAS  PubMed  Google Scholar 

  • Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31:713–727

    CAS  PubMed  Google Scholar 

  • Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85

    CAS  PubMed  Google Scholar 

  • Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453

    CAS  PubMed  Google Scholar 

  • Garrone A, Archipowa N, Zipfel PF, Hermann G, Dietzek B (2015) Plant protochlorophyllide oxidoreductases A and B: catalytic efficiency and initial reaction steps. J Biol Chem 290:28530–28539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giuliani R, Karki S, Covshoff S, Lin HC, Coe RA, Koteyeva NK, Evans MA, Quick WP, von Caemmerer S, Furbank RT, Hibberd JM, Edwards GE, Cousins AB (2019) Transgenic maize phosphoenolpyruvate carboxylase alters leaf-atmosphere CO2 and (13)CO2 exchanges in Oryza sativa. Photosynth Res. https://doi.org/10.1007/s11120-019-00655-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Grossman AR, Bhaya D, Apt KE, Kehoe DM (1995) LIGHT-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Ann Rev Genet 29:231–288

    CAS  PubMed  Google Scholar 

  • Hanada K, Kuromori T, Myouga F, Toyoda T, Li WH, Shinozaki K (2009) Evolutionary persistence of functional compensation by duplicate genes in Arabidopsis. Genome Biol Evol 1:409–414

    PubMed  PubMed Central  Google Scholar 

  • He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, Lopez-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand S, Xenarios I, Fankhauser C (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711

    CAS  PubMed  Google Scholar 

  • Hufford MB, Xu X, van Heerwaarden J, Pyhajarvi T, Chia JM, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM, Lai J, Morrell PL, Shannon LM, Song C, Springer NM, Swanson-Wagner RA, Tiffin P, Wang J, Zhang G, Doebley J, McMullen MD, Ware D, Buckler ES, Yang S, Ross-Ibarra J (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen RG (1983) Photosynthesis: C3, C4. mechanisms, and cellular and environmental regulation, of photosynthesis. Science 222:1009–1009

    CAS  PubMed  Google Scholar 

  • Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045

    CAS  PubMed  Google Scholar 

  • Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361

    CAS  PubMed  Google Scholar 

  • Kaur N, Li J, Hu J (2013) Peroxisomes and Photomorphogenesis. In: del Río LA (ed) Peroxisomes and their Key Role in Cellular Signaling and Metabolism. Springer, Netherlands, Dordrecht, pp 195–211

    Google Scholar 

  • Kim B, Jeong YJ, Corvalan C, Fujioka S, Cho S, Park T, Choe S (2014) Darkness and gulliver2/phyB mutation decrease the abundance of phosphorylated BZR1 to activate brassinosteroid signaling in Arabidopsis. Plant J 77:737–747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357

    CAS  PubMed  Google Scholar 

  • Kuhlgert S, Austic G, Zegarac R, Osei-Bonsu I, Hoh D, Chilvers MI, Roth MG, Bi K, TerAvest D, Weebadde P, Kramer DM (2016) MultispeQ Beta: a tool for large-scale plant phenotyping connected to the open PhotosynQ network. R Soc Open Sci 3:160592

    PubMed  PubMed Central  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559

    PubMed  PubMed Central  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    PubMed  PubMed Central  Google Scholar 

  • Li T, Jia KP, Lian HL, Yang X, Li L, Yang HQ (2014) Jasmonic acid enhancement of anthocyanin accumulation is dependent on phytochrome A signaling pathway under far-red light in Arabidopsis. Biochem Biophys Res Commun 454:78–83

    CAS  PubMed  Google Scholar 

  • Li QF, Huang LC, Wei K, Yu JW, Zhang CQ, Liu QQ (2017) Light involved regulation of BZR1 stability and phosphorylation status to coordinate plant growth in Arabidopsis. Biosci Rep. https://doi.org/10.1042/BSR20170069

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu M, Yang G, Li P, Wang Z, Fu S, Zhang X, Chen X, Shi M, Ming Z, Xia J (2018) Bioinformatic and functional analysis of a key determinant underlying the substrate selectivity of the Al transporter, Nrat1. Front Plant Sci 9:606

    PubMed  PubMed Central  Google Scholar 

  • Luo XM, Lin WH, Zhu S, Zhu JY, Sun Y, Fan XY, Cheng M, Hao Y, Oh E, Tian M, Liu L, Zhang M, Xie Q, Chong K, Wang ZY (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19:872–883

    CAS  PubMed  PubMed Central  Google Scholar 

  • Menon C, Sheerin DJ, Hiltbrunner A (2016) SPA proteins: SPAnning the gap between visible light and gene expression. Planta 244:297–312

    CAS  PubMed  Google Scholar 

  • Miao Z, Han Z, Zhang T, Chen S, Ma C (2017) A systems approach to a spatio-temporal understanding of the drought stress response in maize. Sci Rep 7:6590

    PubMed  PubMed Central  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    CAS  PubMed  Google Scholar 

  • Okada K (2009) PetH is rate-controlling in the interaction between PetH, a component of the supramolecular complex with photosystem II, and PetF, a light-dependent electron transfer protein. Biochem Biophys Res Commun 389:394–398

    CAS  PubMed  Google Scholar 

  • Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pahari S, Cormark RD, Blackshaw MT, Liu C, Erickson JL, Schultz EA (2014) Arabidopsis UNHINGED encodes a VPS51 homolog and reveals a role for the GARP complex in leaf shape and vein patterning. Development 141:1894–1905

    CAS  PubMed  Google Scholar 

  • Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parks BM (2003) The red side of photomorphogenesis. Plant Physiol 133:1437–1444

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ponnu J, Wahl V, Schmid M (2011) Trehalose-6-phosphate: connecting plant metabolism and development. Front Plant Sci 2:70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    CAS  PubMed  Google Scholar 

  • Sakata S, Mizusawa N, Kubota-Kawai H, Sakurai I, Wada H (2013) Psb28 is involved in recovery of photosystem II at high temperature in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1827:50–59

    CAS  PubMed  Google Scholar 

  • Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119

    CAS  PubMed  Google Scholar 

  • Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci USA 108:4069–4074

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schottler MA, Toth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5:188

    PubMed  PubMed Central  Google Scholar 

  • Schottler MA, Toth SZ, Boulouis A, Kahlau S (2015) Photosynthetic complex stoichiometry dynamics in higher plants: biogenesis, function, and turnover of ATP synthase and the cytochrome b6f complex. J Exp Bot 66:2373–2400

    PubMed  Google Scholar 

  • Schumann T, Paul S, Melzer M, Dormann P, Jahns P (2017) Plant growth under natural light conditions provides highly flexible short-term acclimation properties toward high light stress. Front Plant Sci 8:681

    PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi Q, Kong F, Zhang H, Ye J, Heng S, Liang R, Ma L, Liu J, Lu X, Li P, Li G (2019) Molecular mechanisms governing shade responses in maize. Biochem Biophys Res Commun 516:112–119

    CAS  PubMed  Google Scholar 

  • Shikanai T (2016) Chloroplast NDH: A different enzyme with a structure similar to that of respiratory NADH dehydrogenase. Biochim Biophys Acta 1857:1015–1022

    CAS  PubMed  Google Scholar 

  • Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98

    CAS  PubMed  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Wu G, Zhao B, Wang B, Lang Z, Zhang C, Wang H (2016) Regulatory modules controlling early shade avoidance response in maize seedlings. BMC Genomics 17:269

    PubMed  PubMed Central  Google Scholar 

  • Wang B, Lin Z, Li X, Zhao Y, Zhao B, Wu G, Ma X, Wang H, Xie Y, Li Q, Song G, Kong D, Zheng Z, Wei H, Shen R, Wu H, Chen C, Meng Z, Wang T, Li Y, Li X, Chen Y, Lai J, Hufford MB, Ross-Ibarra J, He H, Wang H (2020) Genome-wide selection and genetic improvement during modern maize breeding. Nat Genet. https://doi.org/10.1038/s41588-020-0616-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weise SE, Weber AP, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218:474–482

    CAS  PubMed  Google Scholar 

  • Wise RR, Hoober JK (2006) The Diversity of Plastid Form and Function. Springer, The Netherlands, pp 3–26

    Google Scholar 

  • Wu SH (2014) Gene expression regulation in photomorphogenesis from the perspective of the central dogma. Annu Rev Plant Biol 65:311–333

    CAS  PubMed  Google Scholar 

  • Yilmaz A, Nishiyama MY Jr, Fuentes BG, Souza GM, Janies D, Gray J, Grotewold E (2009) GRASSIUS: a platform for comparative regulatory genomics across the grasses. Plant Physiol 149:171–180

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J (2012) Genetic Redundancies and Their Evolutionary Maintenance. In: Soyer OS (ed) Evolutionary Systems Biology. Springer, New York , pp 279–300

    Google Scholar 

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Acknowledgements

This study was funded by the Young Scientists Fund of the National Natural Science Foundation of China (Grant No. 31701438) and the Science Foundation for Post Doctorate Research of the Ministry of Science and Technology of China (2018M633588).

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Shutu Xu, Dongwei Guo and Jiquan Xue conceived and designed the experiments. Shutu Xu, Xiaonan Gou, Wenxin Zhang, Ting Li and Jianzhou Qu performed experiments. Jianzhou Qu analyzed and interpreted the data. Jianzhou Qu and Shutu Xu wrote the paper and prepared figures and/or tables. All authors read and approved the final manuscript.

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Correspondence to Jiquan Xue.

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438_2021_1761_MOESM1_ESM.tif

Supplementary Correlation of gene expression level across replicates. For each gene, the expression values were normalized by the log2(FPKM+1). The scale bar shows the degree of correlation between samples. The samples from seedlings under normal light condition (SNL), seedlings after four days of dark treatment (SDT) and four days after seedlings return to normal light (SRNL) (TIF 2312 KB)

438_2021_1761_MOESM2_ESM.tif

Supplementary Comparison of expression patterns of candidate genes by qRT-PCR and RNA-Seq. Histogram showing expression levels of candidate genes based on qRT-PCR (left). Boxplot showing expression levels of candidate genes based on RNA-Seq (right). The samples from seedlings under normal light condition (SNL), seedlings after four days of dark treatment (SDT) and four days after seedlings return to normal light (SRNL) (TIF 3827 KB)

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Qu, J., Gou, X., Zhang, W. et al. New insights into the response of maize to fluctuations in the light environment. Mol Genet Genomics 296, 615–629 (2021). https://doi.org/10.1007/s00438-021-01761-6

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