Abstract
The Lateral Organ Boundaries Domain (LBD) proteins are a class of plant-specific transcription factor family, which participate in plant growth, development, and stress response. In present study, 61 PheLBD genes were identified in moso bamboo (Phyllostachys edulis) genome. These members clustered into two major classes (Class I and Class II) based on the previous study and phylogenetic analysis, and Class I was further divided into five subgroups (Class I–Class E). The gene architecture and conserved motifs suggested the members in one subgroup shared the structural similarities and highly conserved motif compositions. Scaffold position analysis showed PheLBDs were unevenly located on 19 moso bamboo scaffolds. Synteny analysis indicated segmental duplication and transposed duplication played significant roles in PheLBD gene expansion and some PheLBD genes have been and are undergoing markedly positive purifying selection during evolution. A large number of light-responsive elements, abiotic-stress and hormone-response elements were discovered in the promoter of PheLBDs. Public RNA-seq data helps to analyze the expression profile of PheLBD genes in 14 moso bamboo tissues. And we also found most genes in class II were significantly up-regulated under auxin naphthaleneacetic acid (NAA) treatment, but were sensitive after Gibberellins (GA)-treated. Moreover, quantitative real-time reverse transcription PCR (RT-qPCR) analysis showed that PheLBDs have different response to salt and drought stress as well as abscisic acid (ABA) and Methyl jasmonate (MeJA). Overall, these results paved a way for the further functional studies of PheLBDs.
Similar content being viewed by others
References
Ariel FD, Diet A, Crespi M, Chan RL (2010) The LOB-like transcription factor Mt LBD1 controls Medicago truncatula root architecture under salt stress. Plant Signal Behav 5(12):1666–1668
Bailey TL, Nadya W, Chris M, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373
Berckmans B, Vassileva V, Schmid SPC, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei CLA, Koncz C, Bogre L, Persiau G, De Jaeger G, Friml J, Simon R, Beeckman T, De Veylder L (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23(10):3671–3683. https://doi.org/10.1105/tpc.111.088377
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Cao H, Liu CY, Liu CX, Zhao YL, Xu RR (2016) Genomewide analysis of the lateral organ boundaries domain gene family in Vitis vinifera. J Genet 95(3):515–526. https://doi.org/10.1007/s12041-016-0660-z
Chen DM, Chen Z, Wu M, Wang Y, Wang YJ, Yan HW, Xiang Y (2017) Genome-wide identification and expression analysis of the HD-Zip gene family in moso bamboo (Phyllostachys edulis). J Plant Growth Regul 36(2):323–337. https://doi.org/10.1007/s00344-016-9642-x
Chen C, Chen H, Zhang Y, Thomas HR, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Cheng T, Fu B, Wu Y, Long R, Xia Q (2015) Transcriptome Sequencing and Positive Selected Genes Analysis of Bombyx mandarina. PLoS ONE 10(3):e0122837
Chou KC, Shen HB (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5(6):e11335
Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer ELL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251. https://doi.org/10.1093/nar/gkj149
Finn RD, Penelope C, Eberhardt RY, Eddy SR, Jaina M, Mitchell AL, Potter SC, Marco P, Matloob Q, Amaia SV (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res D1:D279–D285
Gao Y, Liu H, Zhang K, Li F, Xiang Y (2020) A moso bamboo transcription factor, Phehdz1, positively regulates the drought stress response of transgenic rice. Plant Cell Reports 40(1):187–204. https://doi.org/10.1007/s00299-020-02625-w
Ge X, Zhou B, Wang X, Li Q, Cao Y, Gu L (2018) Imposed drought effects on carbon storage of moso bamboo ecosystem in southeast China: results from a field experiment. Ecol Res 33:393–402
Gombos M, Zombori Z, Szecsenyi M, Sandor G, Kovacs H, Gyorgyey J (2017) Characterization of the LBD gene family in Brachypodium: a phylogenetic and transcriptional study. Plant Cell Rep 36(1):61–79. https://doi.org/10.1007/s00299-016-2057-0
Gong Z, Xiong L, Shi H, Yang S, Zhu JK (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63(5):635–674. https://doi.org/10.1007/s11427-020-1683-x
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Hereditas 29(8):1023–1026
Guo Z, Xu H, Lei Q, Du J, Li C, Wang C, Yang Y, Yang Y, Sun X (2020) The Arabidopsis transcription factor LBD15 mediates ABA signaling and tolerance of water-deficit stress by regulating ABI4 expression. Plant J 104(2):510–521. https://doi.org/10.1111/tpj.14942
Huang X, Yan H, Liu Y, Yi Y (2020) Genome-wide analysis of lateral organ boundaries domain-in Physcomitrella patens and stress responses. Genes & Genomics 42(6):651–662. https://doi.org/10.1007/s13258-020-00931-x
Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43(5):467–478. https://doi.org/10.1093/pcp/pcf077
Iwakawa H, Iwasaki M, Kojima S, Ueno Y, Soma T, Tanaka H, Semiarti E, Machida Y, Machida C (2007) Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. Plant J 51(2):173–184. https://doi.org/10.1111/j.1365-313X.2007.03132.x
Kim MJ, Kim M, Lee MR, Park SK, Kim J (2015) LATERAL ORGAN BOUNDARIES DOMAIN (LBD) 10 interacts with SIDECAR POLLEN/LBD27 to control pollen development in Arabidopsis. Plant J 81(5):794–809. https://doi.org/10.1111/tpj.12767
Lan YG, Wu L, Wu M, Liu HL, Gao YM, Zhang KM (2020) Xiang Y Transcriptome analysis reveals key genes regulating signaling and metabolic pathways during the growth of moso bamboo (Phyllostachys edulis) shoots. Physiol Plant. https://doi.org/10.1111/ppl.13296
Lee HW, Kim J (2013) EXPANSINA17 Up-Regulated by LBD18/ASL20 promotes lateral root formation during the auxin response. Plant Cell Physiol 54(10):1600–1611. https://doi.org/10.1093/pcp/pct105
Lee DJ, Park JW, Lee HW, Kim J (2009a) Genome-wide analysis of the auxin-responsive transcriptome downstream of iaa1 and its expression analysis reveal the diversity and complexity of auxin-regulated gene expression. J Exp Bot 60(13):3935–3957. https://doi.org/10.1093/jxb/erp230
Lee HW, Kim NY, Lee DJ, Kim J (2009b) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in arabidopsis. Plant Physiol 151(3):1377–1389. https://doi.org/10.1104/pp.109.143685
Lescot M (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327
Liao S, Qin X, Luo L, Han Y, Wang X, Usman B, Nawaz G, Zhao N, Liu Y, Li R (2019) CRISPR/Cas9-induced mutagenesis of semi-rolled leaf 1,2 confers curled leaf phenotype and drought tolerance by influencing protein expression patterns and ROS scavenging in rice (Oryza sativa L.). Agronomy-Basel. https://doi.org/10.3390/agronomy9110728
Liu HL, Ww M, Li F, Gao YM, Chen F, Xiang Y (2018) TCP transcription factors in moso bamboo (Phyllostachys edulis): genome-wide identification and expression analysis. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01263
Liu H, Cao M, Chen X, Ye M, Zhao P, Nan Y, Li W, Zhang C, Kong L, Kong N, Yang C, Chen Y, Wang D, Chen Q (2019b) Genome-wide analysis of the lateral organ boundaries domain (LBD) gene family in solanum tuberosum. Int J Mol Sci. https://doi.org/10.3390/ijms20215360
Liu C, Yu H, Li LG (2019a) SUMO modification of LBD30 by SIZ1 regulates secondary cell wall formation in Arabidopsis thaliana. PLoS Genet. https://doi.org/10.1371/journal.pgen.1007928
Liu L, Zhang J, Xu J, Li Y, Guo L, Wang Z, Zhang X, Zhao B, Guo Y-D, Zhang N (2020) CRISPR/Cas9 targeted mutagenesis of SlLBD40, a lateral organ boundaries domain transcription factor, enhances drought tolerance in tomato. Plant Sci. https://doi.org/10.1016/j.plantsci.2020.110683
Majer C, Hochholdinger F (2011) Defining the boundaries: structure and function of LOB domain proteins. Trends Plant Sci 16(1):47–52. https://doi.org/10.1016/j.tplants.2010.09.009
Marchler-Bauer A, Bo Y, Han LY, He JE, Lanczycki CJ, Lu SN, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang ZX, Yamashita RA, Zhang DC, Zheng CJ, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203. https://doi.org/10.1093/nar/gkw1129
Matsumura Y, Iwakawa H, Machida Y, Machida C (2009) Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members. Plant J 58(3):525–537. https://doi.org/10.1111/j.1365-313X.2009.03797.x
Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17(2):444–463
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19(1):118–130. https://doi.org/10.1105/tpc.106.047761
Peng Z, Lu Y, Li L, Zhao Q, Feng Q, Gao Z, Lu H, Hu T, Yao N, Liu K, Li Y, Fan D, Guo Y, Li W, Lu Y, Weng Q, Zhou C, Zhang L, Huang T, Zhao Y, Zhu C, Liu X, Yang X, Wang T, Miao K, Zhuang C, Cao X, Tang W, Liu G, Liu Y, Chen J, Liu Z, Yuan L, Liu Z, Huang X, Lu T, Fei B, Ning Z, Han B, Jiang Z (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45(4):456–461. https://doi.org/10.1038/ng.2569
Qiao X, Li QH, Yin H, Qi KJ, Li LT, Wang RZ, Zhang SL, Paterson AH (2019) Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biol. https://doi.org/10.1186/s13059-019-1650-2
Qi-Jiang HE, Wang KH, Weng PJ, Rong WU (2001) Preliminary report on experiment of watering bamboo stand for shoot. J Zhejiang Forest Sci Technol 2001(05):18–20
Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in arabidopsis. Plant Cell 21(11):3567–3584
Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y (2001) The asymmetric leaves2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128(10):1771–1783
Shuai B, Reynaga-Pena CG, Springer PS (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129(2):747–761. https://doi.org/10.1104/pp.010926
Song BB, Tang ZK, Li XL, Li JM, Zhang MY, Zhao KJ, Liu HN, Zhang SL, Wu J (2020) Mining and evolution analysis of lateral organ boundaries domain (LBD) genes in Chinese white pear (Pyrus bretschneideri). BMC Genomics. https://doi.org/10.1186/s12864-020-06999-9
Sun XD, Feng ZH, Meng LS, Zhu J, Geitmann A (2013) Arabidopsis ASL11/LBD15 is involved in shoot apical meristem development and regulates WUS expression. Planta 237(5):1367–1378. https://doi.org/10.1007/s00425-013-1844-x
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Thatcher LF, Powell JJ, Aitken EAB, Kazan K, Manners JM (2012) The lateral organ boundaries domain transcription factor LBD20 functions in fusarium wilt susceptibility and jasmonate signaling in arabidopsis. Plant Physiol 160(1):407–418. https://doi.org/10.1104/pp.112.199067
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):1673–1680
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Tae-Ho L, Jin H, Barry M, Guo H (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7):e49–e49
Wang X, Zhang S, Su L, Liu X, Hao Y (2013) A genome-wide analysis of the LBD (LATERAL ORGAN BOUNDARIES Domain) gene family in malus domestica with a functional characterization of MdLBD11. Plos One 8(2):e57044. https://doi.org/10.1371/journal.pone.0057044
Wang W, Gu L, Ye S, Zhang H, Cai C, Xiang M, Gao Y, Wang Q, Lin C, Zhu Q (2017) Genome-wide analysis and transcriptomic profiling of the auxin biosynthesis, transport and signaling family genes in moso bamboo (Phyllostachys heterocycla). BMC Genomics 18(1):870
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Hochstrasser DF (1999) Protein Identification and Analysis Tools in the ExPASy Server. Methods Mol Biol 112(112):531–552
Xu C, Cao HF, Zhang QQ, Wang HZ, Xin W, Xu EJ, Zhang SQ, Yu RX, Yu DX, Hu YX (2018) Control of auxin-induced callus formation by bZIP59-LBD complex in Arabidopsis regeneration. Nature Plants 4(2):108–115. https://doi.org/10.1038/s41477-017-0095-4
Yang Y, Yu XB, Wu P (2006) Comparison and evolution analysis of two rice subspecies LATERAL ORGAN BOUNDARIES domain gene family and their evolutionary characterization from Arabidopsis. Mol Phylogenet Evol 39(1):248–262. https://doi.org/10.1016/j.ympev.2005.09.016
Yang TQ, Fang GY, He H, Chen JH (2016) Genome-wide identification, evolutionary analysis and expression profiles of LATERAL ORGAN BOUNDARIES DOMAIN gene family in Lotus japonicus and Medicago truncatula. Plos One. 11(8):e0161901. https://doi.org/10.1371/journal.pone.0161901
Yoko Okushima HF, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 Regulate Lateral Root Formation via Direct Activation of LBD/ASL Genes in Arabidopsis. Plant Cell 19(1):118–130
Yordanov YS (2010) Regan, Busov (2010) Members of the LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in populus. Plant Cell 22(11):3662–3677
Zhang YM, Zhang SZ, Zheng CC (2014) Genomewide analysis of LATERAL ORGAN BOUNDARIES Domain gene family in Zea mays. J Genet 93(1):79–91. https://doi.org/10.1007/s12041-014-0342-7
Zhang H, Wang H, Qiang Z, Gao Y, Wang H, Zhao L, Wang Y, Xi F, Wang W, Yang Y (2018) Transcriptome characterization of moso bamboo (Phyllostachys edulis) seedlings in response to exogenous gibberellin applications. BMC Plant Biol 18(1):125
Zhang X, He Y, He W, Su H, Xu P (2019) Structural and functional insights into the LBD family involved in abiotic stress and flavonoid synthases in Camellia sinensis. Sci Rep 9(1):15651. https://doi.org/10.1038/s41598-019-52027-6
Zhao H, Gao Z, Wang L, Wang J, Wang S, Fei B, Chen C, Shi C, Liu X, Zhang H, Lou Y, Chen L, Sun H, Zhou X, Wang S, Zhang C, Xu H, Li L, Yang Y, Wei Y, Yang W, Gao Q, Yang H, Zhao S, Jiang Z (2018) Chromosome-level reference genome and alternative splicing atlas of moso bamboo (Phyllostachys edulis). Gigascience. https://doi.org/10.1093/gigascience/giy115
Zhao J, Gao P, Li C, Lin X, Guo X, Liu S (2019) PhePEBP family genes regulated by plant hormones and drought are associated with the activation of lateral buds and seedling growth in Phyllostachys edulis. Tree Physiol 39:1387–1404
Zhao H, Zhao S, Fei B, Liu H, Yang H, Dai H, Wang D, Jin W, Tang F, Gao Q, Xun H, Wang Y, Qi L, Yue X, Lin S, Gu L, Li L, Zhu T, Wei Q, Su Z, Wan TBWA, Ofori DA, Muthike GM, Mengesha YM, de Castro E Silva RM, Beraldo AL, Gao Z, Liu X, Jiang Z, International Network for B, Rattan (2017) Announcing the Genome Atlas of Bamboo and Rattan (GABR) project: promoting research in evolution and in economically and ecologically beneficial plants. GigaScience 6(7):1–7. https://doi.org/10.1093/gigascience/gix046
Zhu QH, Guo AY, Gao G, Zhong YF, Xu M, Huang MR, Luo JC (2007) DPTF: a database of poplar transcription factors. Bioinformatics 23(10):1307–1308. https://doi.org/10.1093/bioinformatics/btm113
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31670672), Postdoctoral Science Foundation of China (2019M652166), the Graduate Innovation Fund from Anhui Agricultural University (2020ysj-55) and Project of introducing and stabilizing talents in Anhui Agricultural University (yj2019-10).
Author information
Authors and Affiliations
Contributions
YMG participated in the revision of the manuscript, KW wrote the draft manuscript and conceived main frame of this study, RJW processed the experimental data, LNW and HXL designed and performed experiments, MW assisted to complete the writing of this paper, YX, the correspondence author, provided financial support for the article and designed the way and frame of this research. All authors read and approved the revised manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors have no conflicts of interest to declare.
Additional information
Handling Editor: Václav Motyka.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gao, Y., Wang, K., Wang, R. et al. Identification and Expression Analysis of LBD Genes in Moso Bamboo (Phyllostachys edulis). J Plant Growth Regul 41, 2798–2817 (2022). https://doi.org/10.1007/s00344-021-10475-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10475-3