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A genome-wide approach to the systematic and comprehensive analysis of LIM gene family in sorghum (Sorghum bicolor L.)

  • Md. Abdur Rauf Sarkar (Department of Genetic Engineering and Biotechnology, Faculty of Biological Science and Technology, Jashore University of Science and Technology) ;
  • Salim Sarkar (Department of Genetic Engineering and Biotechnology, Faculty of Biological Science and Technology, Jashore University of Science and Technology) ;
  • Md Shohel Ul Islam (Department of Genetic Engineering and Biotechnology, Faculty of Biological Science and Technology, Jashore University of Science and Technology) ;
  • Fatema Tuz Zohra (Department of Genetic Engineering and Biotechnology, Faculty of Biological Sciences, University of Rajshahi) ;
  • Shaikh Mizanur Rahman (Department of Genetic Engineering and Biotechnology, Faculty of Biological Science and Technology, Jashore University of Science and Technology)
  • Received : 2023.02.02
  • Accepted : 2023.08.09
  • Published : 2023.09.30

Abstract

The LIM domain-containing proteins are dominantly found in plants and play a significant role in various biological processes such as gene transcription as well as actin cytoskeletal organization. Nevertheless, genome-wide identification as well as functional analysis of the LIM gene family have not yet been reported in the economically important plant sorghum (Sorghum bicolor L.). Therefore, we conducted an in silico identification and characterization of LIM genes in S. bicolor genome using integrated bioinformatics approaches. Based on phylogenetic tree analysis and conserved domain, we identified five LIM genes in S. bicolor (SbLIM) genome corresponding to Arabidopsis LIM (AtLIM) genes. The conserved domain, motif as well as gene structure analyses of the SbLIM gene family showed the similarity within the SbLIM and AtLIM members. The gene ontology (GO) enrichment study revealed that the candidate LIM genes are directly involved in cytoskeletal organization and various other important biological as well as molecular pathways. Some important families of regulating transcription factors such as ERF, MYB, WRKY, NAC, bZIP, C2H2, Dof, and G2-like were detected by analyzing their interaction network with identified SbLIM genes. The cis-acting regulatory elements related to predicted SbLIM genes were identified as responsive to light, hormones, stress, and other functions. The present study will provide valuable useful information about LIM genes in sorghum which would pave the way for the future study of functional pathways of candidate SbLIM genes as well as their regulatory factors in wet-lab experiments.

Keywords

Acknowledgement

The authors are very grateful to the Department of Genetic Engineering and Biotechnology, Faculty of Biological Science and Technology, Jashore University of Science and Technology, Jashore 7408, Bangladesh for providing the opportunity to conduct this research. The authors acknowledge and appreciate the reviewers and the members of the editorial panel for their valuable comments and critical suggestions for improving the quality of this manuscript. The authors wish to thank Mr. Abdul Wahid Dippro, Assistant Professor, Department of English, Faculty of Arts and Social Science, Jashore University of Science and Technology, Jashore 7408, Bangladesh for extensively editing the manuscript to avoid grammatical errors.

References

  1. Eliasson A, Gass N, Mundel C, Baltz R, Krauter R, Evrard JL, et al. Molecular and expression analysis of a LIM protein gene family from flowering plants. Mol Gen Genet 2000;264:257-267. https://doi.org/10.1007/s004380000312
  2. Way JC, Chalfie M. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 1988;54:5-16. https://doi.org/10.1016/0092-8674(88)90174-2
  3. Kawaoka A, Ebinuma H. Transcriptional control of lignin biosynthesis by tobacco LIM protein. Phytochemistry 2001;57:1149-1157. https://doi.org/10.1016/S0031-9422(01)00054-1
  4. Maul RS, Song Y, Amann KJ, Gerbin SC, Pollard TD, Chang DD. EPLIN regulates actin dynamics by cross-linking and stabilizing filaments. J Cell Biol 2003;160:399-407. https://doi.org/10.1083/jcb.200212057
  5. Dawid IB, Breen JJ, Toyama R. LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet 1998;14:156-162. https://doi.org/10.1016/S0168-9525(98)01424-3
  6. Dawid IB, Toyama R, Taira M. LIM domain proteins. C R Acad Sci III 1995;318:295-306.
  7. Labalette C, Nouet Y, Levillayer F, Colnot S, Chen J, Claude V, et al. Deficiency of the LIM-only protein FHL2 reduces intestinal tumorigenesis in Apc mutant mice. PLoS One 2010;5:e10371.
  8. Baltz R, Evrard JL, Domon C, Steinmetz A. A LIM motif is present in a pollen-specific protein. Plant Cell 1992;4:1465-1466.
  9. Papuga J, Thomas C, Dieterle M, Moreau F, Steinmetz A. Arabidopsis LIM domain proteins involved in actin bundling exhibit different modes of regulation. FEBS J 2009;276:245.
  10. Thomas C, Hoffmann C, Dieterle M, Van Troys M, Ampe C, Steinmetz A. Tobacco WLIM1 is a novel F-actin binding protein involved in actin cytoskeleton remodeling. Plant Cell 2006; 18:2194-2206. https://doi.org/10.1105/tpc.106.040956
  11. Khatun K, Robin AH, Park JI, Ahmed NU, Kim CK, Lim KB, et al. Genome-wide identification, characterization and expression profiling of LIM family genes in Solanum lycopersicum L. Plant Physiol Biochem 2016;108:177-190. https://doi.org/10.1016/j.plaphy.2016.07.006
  12. Li Y, Jiang J, Li L, Wang XL, Wang NN, Li DD, et al. A cotton LIM domain-containing protein (GhWLIM5) is involved in bundling actin filaments. Plant Physiol Biochem 2013;66:34-40. https://doi.org/10.1016/j.plaphy.2013.01.018
  13. Arnaud D, Dejardin A, Leple JC, Lesage-Descauses MC, Pilate G. Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Res 2007;14: 103-116. https://doi.org/10.1093/dnares/dsm013
  14. Zhao M, He L, Gu Y, Wang Y, Chen Q, He C. Genome-wide analyses of a plant-specific LIM-domain gene family implicate its evolutionary role in plant diversification. Genome Biol Evol 2014;6:1000-1012. https://doi.org/10.1093/gbe/evu076
  15. Srivastava V, Verma PK. The plant LIM proteins: unlocking the hidden attractions. Planta 2017;246:365-375. https://doi.org/10.1007/s00425-017-2715-7
  16. Kawaoka A, Kaothien P, Yoshida K, Endo S, Yamada K, Ebinuma H. Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J 2000;22:289-301. https://doi.org/10.1046/j.1365-313x.2000.00737.x
  17. Han LB, Li YB, Wang HY, Wu XM, Li CL, Luo M, et al. The dual functions of WLIM1a in cell elongation and secondary wall formation in developing cotton fibers. Plant Cell 2013;25:4421-4438. https://doi.org/10.1105/tpc.113.116970
  18. Yang S, Zhu G, Wang C, Chen L, Song Y, Wang J. Regulation of secondary xylem formation in young hybrid poplars by modifying the expression levels of the PtaGLIMa gene. Mol Breed 2017;37:124.
  19. Sala S, Ampe C. An emerging link between LIM domain proteins and nuclear receptors. Cell Mol Life Sci 2018;75:1959-1971. https://doi.org/10.1007/s00018-018-2774-3
  20. Zheng Q, Zhao Y. The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein-protein interaction. Biol Cell 2007;99:489-502. https://doi.org/10.1042/BC20060126
  21. Papuga J, Hoffmann C, Dieterle M, Moes D, Moreau F, Tholl S, et al. Arabidopsis LIM proteins: a family of actin bundlers with distinct expression patterns and modes of regulation. Plant Cell 2010;22:3034-3052. https://doi.org/10.1105/tpc.110.075960
  22. Wang C, Zhang LJ, Huang RD. Cytoskeleton and plant salt stress tolerance. Plant Signal Behav 2011;6:29-31. https://doi.org/10.4161/psb.6.1.14202
  23. Wang Y, Liu GJ, Yan XF, Wei ZG, Xu ZR. MeJA-inducible expression of the heterologous JAZ2 promoter from Arabidopsis in Populus trichocarpa protoplasts. J Plant Dis Prot 2011;118:69-74. https://doi.org/10.1007/BF03356384
  24. Wasteneys GO, Yang Z. The cytoskeleton becomes multidisciplinary. Plant Physiol 2004;136:3853-3854. https://doi.org/10.1104/pp.104.900130
  25. Baltz R, Schmit AC, Kohnen M, Hentges F, Steinmetz A. Differential localization of the LIM domain protein PLIM-1 in microspores and mature pollen grains from sunflower. Sex Plant Reprod 1999;12:60-65. https://doi.org/10.1007/s004970050172
  26. Moes D, Gatti S, Hoffmann C, Dieterle M, Moreau F, Neumann K, et al. A LIM domain protein from tobacco involved in actin-bundling and histone gene transcription. Mol Plant 2013;6: 483-502. https://doi.org/10.1093/mp/sss075
  27. Chen F, Hu Y, Vannozzi A, Wu K, Cai H, Qin Y, et al. The WRKY transcription factor family in model plants and crops. Crit Rev Plant Sci 2017;36:311-335. https://doi.org/10.1080/07352689.2018.1441103
  28. Zhao ZY, Che P, Glassman K, Albertsen M. Nutritionally enhanced sorghum for the arid and semiarid tropical areas of Africa. Methods Mol Biol 2019;1931:197-207. https://doi.org/10.1007/978-1-4939-9039-9_14
  29. Pelpolage SW, Han K, Koaze H, Hamamoto T, Hoshizawa M, Fukushima M. Influence of enzyme-resistant fraction of sorghum (Sorghum bicolor L.) flour on gut microflora composition, short chain fatty acid production and toxic substance metabolism. J Food Nutr Res 2019;58:135-145.
  30. Xiong Y, Zhang P, Warner RD, Fang Z. Sorghum grain: from genotype, nutrition, and phenolic profile to its health benefits and food applications. Compr Rev Food Sci Food Saf 2019;18:2025-2046. https://doi.org/10.1111/1541-4337.12506
  31. USDA. Quick Stats. Washington, DC: United States Department of Agriculture, Natioanl Agricultural Statistics Service, 2019. Accessed 2023 Feb 2. Available from: https://quickstats.nass.usda.gov/.
  32. Han Y, Song L, Liu S, Zou N, Li Y, Qin Y, et al. Simultaneous determination of 124 pesticide residues in Chinese liquor and liquor-making raw materials (sorghum and rice hull) by rapid Multi-plug Filtration Cleanup and gas chromatography-tandem mass spectrometry. Food Chem 2018;241:258-267. https://doi.org/10.1016/j.foodchem.2017.08.103
  33. Prasad PV, Djanaguiraman M, Perumal R, Ciampitti IA. Impact of high temperature stress on floret fertility and individual grain weight of grain sorghum: sensitive stages and thresholds for temperature and duration. Front Plant Sci 2015;6:820.
  34. Prasad PV, Pisipati SR, Mutava RN, Tuinstra MR. Sensitivity of grain sorghum to high temperature stress during reproductive development. Crop Sci 2008;48:1911-1917. https://doi.org/10.2135/cropsci2008.01.0036
  35. Rooney WL. Sorghum improvement: integrating traditional and new technology to produce improved genotypes. Adv Agron 2004;83:37-109. https://doi.org/10.1016/S0065-2113(04)83002-5
  36. Tsuji W, Ali ME, Inanaga S, Sygimoto Y. Growth and gas exchange of three sorghum cultivars under drought stress. Biol Plant 2003;46:583-587. https://doi.org/10.1023/A:1024875814296
  37. Li H, Payne WA, Michels GJ, Rush CM. Reducing plant abiotic and biotic stress: drought and attacks of greenbugs, corn leaf aphids and virus disease in dryland sorghum. Environ Exp Bot 2008;63:305-316. https://doi.org/10.1016/j.envexpbot.2007.11.014
  38. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. The Sorghum bicolor genome and the diversification of grasses. Nature 2009;457:551-556. https://doi.org/10.1038/nature07723
  39. Yang R, Chen M, Sun JC, Yu Y, Min DH, Chen J, et al. Genome-wide analysis of LIM family genes in foxtail millet (Setaria italica L.) and characterization of the role of SiWLIM2b in drought tolerance. Int J Mol Sci 2019;20:1303.
  40. Park JI, Ahmed NU, Jung HJ, Arasan SK, Chung MY, Cho YG, et al. Identification and characterization of LIM gene family in Brassica rapa. BMC Genomics 2014;15:641.
  41. Cheng X, Li G, Muhammad A, Zhang J, Jiang T, Jin Q, et al. Molecular identification, phylogenomic characterization and expression patterns analysis of the LIM (LIN-11, Isl1 and MEC-3 domains) gene family in pear (Pyrus bretschneideri) reveal its potential role in lignin metabolism. Gene 2019;686:237-249. https://doi.org/10.1016/j.gene.2018.11.064
  42. Arnaud D, Dejardin A, Leple JC, Lesage-Descauses MC, Boizot N, Villar M, et al. Expression analysis of LIM gene family in poplar, toward an updated phylogenetic classification. BMC Res Notes 2012;5:102.
  43. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406-425.
  44. Sievers F, Higgins DG. Clustal Omega for making accurate alignments of many protein sequences. Protein Sci 2018;27:135-145. https://doi.org/10.1002/pro.3290
  45. Tajima F, Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1984;1:269-285.
  46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997;25:4876-4882. https://doi.org/10.1093/nar/25.24.4876
  47. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680. https://doi.org/10.1093/nar/22.22.4673
  48. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021;38:3022-3027. https://doi.org/10.1093/molbev/msab120
  49. Bailey TL, Johnson J, Grant CE, Noble WS. The MEME suite. Nucleic Acids Res 2015;43:W39-W49. https://doi.org/10.1093/nar/gkv416
  50. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 2015;31: 1296-1297. https://doi.org/10.1093/bioinformatics/btu817
  51. Chao JT, Kong YZ, Wang Q, Sun YH, Gong DP, Lv J, et al. MapGene2Chrom, a tool to draw gene physical map based on Perl and SVG languages. Yi Chuan 2015;37:91-97.
  52. Liu L, Zhang Z, Mei Q, Chen M. PSI: a comprehensive and integrative approach for accurate plant subcellular localization prediction. PLoS One 2013;8:e75826.
  53. Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, et al. PlantTFDB 4. 0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 2017;45:D1040-D1045. https://doi.org/10.1093/nar/gkw982
  54. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003;13:2498-2504. https://doi.org/10.1101/gr.1239303
  55. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 2002;30:325-327. https://doi.org/10.1093/nar/30.1.325
  56. Shen XX, Salichos L, Rokas A. A genome-scale investigation of how sequence, function, and tree-based gene properties influence phylogenetic inference. Genome Biol Evol 2016;8:2565-2580. https://doi.org/10.1093/gbe/evw179
  57. Shaul O. How introns enhance gene expression. Int J Biochem Cell Biol 2017;91:145-155. https://doi.org/10.1016/j.biocel.2017.06.016
  58. Castle WE. Mendel's Law of Heredity. Science 1903;18:396-406. https://doi.org/10.1126/science.18.456.396
  59. Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R. Gene duplication as a major force in evolution. J Genet 2013; 92:155-161. https://doi.org/10.1007/s12041-013-0212-8
  60. Ehrlich JS, Hansen MD, Nelson WJ. Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev Cell 2002;3:259-270. https://doi.org/10.1016/S1534-5807(02)00216-2
  61. Glory E, Murphy RF. Automated subcellular location determination and high-throughput microscopy. Dev Cell 2007;12:7-16. https://doi.org/10.1016/j.devcel.2006.12.007
  62. Thaler JP, Lee SK, Jurata LW, Gill GN, Pfaff SL. LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 2002;110:237-249. https://doi.org/10.1016/S0092-8674(02)00823-1
  63. Khan SA, Li MZ, Wang SM, Yin HJ. Revisiting the role of plant transcription factors in the battle against abiotic stress. Int J Mol Sci 2018;19:1634.
  64. Latchman DS. Transcription factors: an overview. Int J Biochem Cell Biol 1997;29:1305-1312. https://doi.org/10.1016/S1357-2725(97)00085-X
  65. Lutova LA, Dodueva IE, Lebedeva MA, Tvorogova VE. Transcription factors in developmental genetics and the evolution of higher plants. Genetika 2015;51:539-557.
  66. Sasaki K. Utilization of transcription factors for controlling floral morphogenesis in horticultural plants. Breed Sci 2018;68:88-98. https://doi.org/10.1270/jsbbs.17114
  67. Shu Y, Liu Y, Zhang J, Song L, Guo C. Genome-wide analysis of the AP2/ERF superfamily genes and their responses to abiotic stress in Medicago truncatula. Front Plant Sci 2015;6:1247.
  68. Mengiste T, Chen X, Salmeron J, Dietrich R. The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 2003;15:2551-2565. https://doi.org/10.1105/tpc.014167
  69. Meshi T, Iwabuchi M. Plant transcription factors. Plant Cell Physiol 1995;36:1405-1420.
  70. Muller M, Munne-Bosch S. Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 2015;169:32-41. https://doi.org/10.1104/pp.15.00677
  71. Xie Z, Nolan TM, Jiang H, Yin Y. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front Plant Sci 2019;10:228.
  72. Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G. An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 2012;31:349-360. https://doi.org/10.1007/s00299-011-1170-3
  73. Cao Y, Li K, Li Y, Zhao X, Wang L. MYB transcription factors as regulators of secondary metabolism in plants. Biology (Basel) 2020;9:61.
  74. Ramya M, Kwon OK, An HR, Park PM, Baek YS, Park PH. Floral scent: regulation and role of MYB transcription factors. Phytochem Lett 2017;19:114-120. https://doi.org/10.1016/j.phytol.2016.12.015
  75. Cao H, Huang P, Zhang L, Shi Y, Sun D, Yan Y, et al. Characterization of 47 Cys2 -His2 zinc finger proteins required for the development and pathogenicity of the rice blast fungus Magnaporthe oryzae. New Phytol 2016;211:1035-1051. https://doi.org/10.1111/nph.13948
  76. Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, et al. Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 2012;19:463-476. https://doi.org/10.1093/dnares/dss026
  77. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, et al. bZIP transcription factors in Arabidopsis. Trends Plant Sci 2002;7:106-111. https://doi.org/10.1016/S1360-1385(01)02223-3
  78. Gupta S, Malviya N, Kushwaha H, Nasim J, Bisht NC, Singh VK, et al. Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 2015;241:549-562. https://doi.org/10.1007/s00425-014-2239-3
  79. Noguero M, Atif RM, Ochatt S, Thompson RD. The role of the DNA-binding One Zinc Finger (DOF) transcription factor family in plants. Plant Sci 2013;209:32-45. https://doi.org/10.1016/j.plantsci.2013.03.016
  80. Azam SM, Liu Y, Rahman ZU, Ali H, Yan C, Wang L, et al. Identification, characterization and expression profiles of Dof transcription factors in pineapple (Ananas comosus L). Trop Plant Biol 2018;11:49-64. https://doi.org/10.1007/s12042-018-9200-8
  81. Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio-Costet MF, et al. Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant 2007;131:434-447. https://doi.org/10.1111/j.1399-3054.2007.00975.x
  82. Oh SK, Baek KH, Park JM, Yi SY, Yu SH, Kamoun S, et al. Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytol 2008;177:977-989. https://doi.org/10.1111/j.1469-8137.2007.02310.x
  83. Shim JS, Jung C, Lee S, Min K, Lee YW, Choi Y, et al. AtMYB44 regulates WRKY70 expression and modulates antagonistic interaction between salicylic acid and jasmonic acid signaling. Plant J 2013;73:483-495. https://doi.org/10.1111/tpj.12051
  84. Guo H, Wang Y, Wang L, Hu P, Wang Y, Jia Y, et al. Expression of the MYB transcription factor gene BplMYB46 affects abiotic stress tolerance and secondary cell wall deposition in Betula platyphylla. Plant Biotechnol J 2017;15:107-121. https://doi.org/10.1111/pbi.12595
  85. Mare C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM, Cattivelli L. Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Mol Biol 2004;55: 399-416. https://doi.org/10.1007/s11103-004-0906-7
  86. Prakash V, Chakraborty S. Identification of transcription factor binding sites on promoter of RNA dependent RNA polymerases (RDRs) and interacting partners of RDR proteins through in silico analysis. Physiol Mol Biol Plants 2019;25:1055-1071. https://doi.org/10.1007/s12298-019-00660-w
  87. Ranty B, Aldon D, Galaud JP. Plant calmodulins and calmodulin-related proteins: multifaceted relays to decode calcium signals. Plant Signal Behav 2006;1:96-104. https://doi.org/10.4161/psb.1.3.2998
  88. Reddy AS, Ali GS, Celesnik H, Day IS. Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 2011;23:2010-2032. https://doi.org/10.1105/tpc.111.084988
  89. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 2000;290:2105-2110. https://doi.org/10.1126/science.290.5499.2105
  90. Xiao Y, You S, Kong W, Tang Q, Bai W, Cai Y, et al. A GARP transcription factor anther dehiscence defected 1 (OsADD1) regulates rice anther dehiscence. Plant Mol Biol 2019;101:403-414. https://doi.org/10.1007/s11103-019-00911-0
  91. Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA. GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 2002;31:713-727. https://doi.org/10.1046/j.1365-313X.2002.01390.x
  92. Jarvis P, Lopez-Juez E. Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 2013;14:787-802. https://doi.org/10.1038/nrm3702
  93. Powell AL, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, et al. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 2012;336:1711-1715. https://doi.org/10.1126/science.1222218
  94. Rossini L, Cribb L, Martin DJ, Langdale JA. The maize golden2 gene defines a novel class of transcriptional regulators in plants. Plant Cell 2001;13:1231-1244. https://doi.org/10.1105/tpc.13.5.1231
  95. Waters MT, Moylan EC, Langdale JA. GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J 2008;56:432-444. https://doi.org/10.1111/j.1365-313X.2008.03616.x
  96. Han XY, Li PX, Zou LJ, Tan WR, Zheng T, Zhang DW, et al. GOLDEN2-LIKE transcription factors coordinate the tolerance to Cucumber mosaic virus in Arabidopsis. Biochem Biophys Res Commun 2016;477:626-632. https://doi.org/10.1016/j.bbrc.2016.06.110
  97. Murmu J, Wilton M, Allard G, Pandeya R, Desveaux D, Singh J, et al. Arabidopsis GOLDEN2-LIKE (GLK) transcription factors activate jasmonic acid (JA)-dependent disease susceptibility to the biotrophic pathogen Hyaloperonospora arabidopsidis, as well as JA-independent plant immunity against the necrotrophic pathogen Botrytis cinerea. Mol Plant Pathol 2014;15:174-184. https://doi.org/10.1111/mpp.12077
  98. Nagatoshi Y, Mitsuda N, Hayashi M, Inoue S, Okuma E, Kubo A, et al. GOLDEN 2-LIKE transcription factors for chloroplast development affect ozone tolerance through the regulation of stomatal movement. Proc Natl Acad Sci U S A 2016;113:4218-4223. https://doi.org/10.1073/pnas.1513093113
  99. Savitch LV, Subramaniam R, Allard GC, Singh J. The GLK1 'regulon' encodes disease defense related proteins and confers resistance to Fusarium graminearum in Arabidopsis. Biochem Biophys Res Commun 2007;359:234-238. https://doi.org/10.1016/j.bbrc.2007.05.084
  100. Schreiber KJ, Nasmith CG, Allard G, Singh J, Subramaniam R, Desveaux D. Found in translation: high-throughput chemical screening in Arabidopsis thaliana identifies small molecules that reduce Fusarium head blight disease in wheat. Mol Plant Microbe Interact 2011;24:640-648. https://doi.org/10.1094/MPMI-09-10-0210
  101. Ng M, Yanofsky MF. Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2001;2:186-195. https://doi.org/10.1038/35056041
  102. Sun W, Jin X, Ma Z, Chen H, Liu M. Basic helix-loop-helix (bHLH) gene family in Tartary buckwheat (Fagopyrum tataricum): genome-wide identification, phylogeny, evolutionary expansion and expression analyses. Int J Biol Macromol 2020; 155:1478-1490. https://doi.org/10.1016/j.ijbiomac.2019.11.126
  103. Zhao R, Song X, Yang N, Chen L, Xiang L, Liu XQ, et al. Expression of the subgroup IIIf bHLH transcription factor CpbHLH1 from Chimonanthus praecox (L.) in transgenic model plants inhibits anthocyanin accumulation. Plant Cell Rep 2020;3 9:891-907. https://doi.org/10.1007/s00299-020-02537-9
  104. Kaur A, Pati PK, Pati AM, Nagpal AK. In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS One 2017;12: e0184523.
  105. Wittkopp PJ, Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 2011;13:59-69. https://doi.org/10.1038/nrg3095
  106. Hidayati N, Anas I. Photosynthesis and transpiration rates of rice cultivated under the system of rice intensification and the effects on growth and yield. Hayati J Biosci 2016;23:67-72. https://doi.org/10.1016/j.hjb.2016.06.002
  107. Lee HW, Cho C, Kim J. Lateral organ boundaries domain16 and 18 act downstream of the AUXIN1 and LIKE-AUXIN3 auxin influx carriers to control lateral root development in Arabidopsis. Plant Physiol 2015;168:1792-1806. https://doi.org/10.1104/pp.15.00578
  108. Gray WM. Hormonal regulation of plant growth and development. PLoS Biol 2004;2:E311.
  109. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S. Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 2003;15:1591-1604. https://doi.org/10.1105/tpc.011650
  110. Shariatipour N, Heidari B. Investigation of drought and salinity tolerance related genes and their regulatory mechanisms in Arabidopsis (Arabidopsis thaliana). Open Bioinform J 2018;11:12-28. https://doi.org/10.2174/1875036201811010012
  111. Zhou Y, Hu L, Wu H, Jiang L, Liu S. Genome-wide identification and transcriptional expression analysis of cucumber superoxide dismutase (SOD) family in response to various abiotic stresses. Int J Genomics 2017;2017:7243973.
  112. Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, et al. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 2002;14:559-574. https://doi.org/10.1105/tpc.010410
  113. Arias JA, Dixon RA, Lamb CJ. Dissection of the functional architecture of a plant defense gene promoter using a homologous in vitro transcription initiation system. Plant Cell 1993;5:485-496.
  114. Li C, Sun Y, Chang Q, Guo C, Bai Y. Bioinformatics and expression pattern analysis of LIM family in wheat. Preprint at: https://doi.org/10.21203/rs.3.rs-1615320/v1 (2022).
  115. Zhu X, Wang B, Wang X, Zhang C, Wei X. Genome-wide identification, characterization and expression analysis of the LIM transcription factor family in quinoa. Physiol Mol Biol Plants 2021;27:787-800. https://doi.org/10.1007/s12298-021-00988-2