Genomics & Informatics

Korea Genome Organization (한국유전체학회)
권호 표지
DOI QR코드

DOI QR Code

A genetic approach to comprehend the complex and dynamic event of floral development: a review

  • Jatindra Nath Mohanty (Department of Botany, School of Applied Sciences, Centurion University of Technology and Management) ;
  • Swayamprabha Sahoo (Centre for Biotechnology, SOA Deemed to be University) ;
  • Puspanjali Mishra (Department of Dietetics & Nutrition, IMS and Sum Hospital, SOA Deemed to be University)
  • Received : 2021.11.30
  • Accepted : 2022.09.17
  • Published : 2022.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

The concepts of phylogeny and floral genetics play a crucial role in understanding the origin and diversification of flowers in angiosperms. Angiosperms evolved a great diversity of ways to display their flowers for reproductive success with variations in floral color, size, shape, scent, arrangements, and flowering time. The various innovations in floral forms and the aggregation of flowers into different kinds of inflorescences have driven new ecological adaptations, speciation, and angiosperm diversification. Evolutionary developmental biology seeks to uncover the developmental and genetic basis underlying morphological diversification. Advances in the developmental genetics of floral display have provided a foundation for insights into the genetic basis of floral and inflorescence evolution. A number of regulatory genes controlling floral and inflorescence development have been identified in model plants such as Arabidopsis thaliana and Antirrhinum majus using forward genetics, and conserved functions of many of these genes across diverse non-model species have been revealed by reverse genetics. Transcription factors are vital elements in systems that play crucial roles in linked gene expression in the evolution and development of flowers. Therefore, we review the sex-linked genes, mostly transcription factors, associated with the complex and dynamic event of floral development and briefly discuss the sex-linked genes that have been characterized through next-generation sequencing.

Keywords

Acknowledgement

We would like to thank IMS and Sum Hospital, SOA Deemed to be University for the facilities. The authors are grateful to President SOA Deemed to be University and CUTM, Bhubaneswar for their constant support and motivations.

References

  1. Ming R, Yu Q, Moore PH. Sex determination in papaya. Semin Cell Dev Biol 2007;18:401-408. https://doi.org/10.1016/j.semcdb.2006.11.013
  2. Renner SS, Ricklefs RE. Dioecy and its correlates in the flowering plants. Am J Bot 1995;82:596-606. https://doi.org/10.1002/j.1537-2197.1995.tb11504.x
  3. Vyskot B, Hobza R. Gender in plants: sex chromosomes are emerging from the fog. Trends Genet 2004;20:432-438. https://doi.org/10.1016/j.tig.2004.06.006
  4. Charlesworth D. Plant sex determination and sex chromosomes. Heredity (Edinb) 2002;88:94-101. https://doi.org/10.1038/sj.hdy.6800016
  5. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, et al. Polyploidy and angiosperm diversification. Am J Bot 2009;96:336-348. https://doi.org/10.3732/ajb.0800079
  6. Zhao D, Yu Q, Chen C, Ma H. Genetic control of reproductive meristems. In: Annual Plant Reviews: Meristematic Tissues in Plant Growth and Development (McManus MT, Veit BE, eds.). Sheffield: Sheffield Academic Press, 2001. pp. 89-142.
  7. Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature 1991;353:31-37. https://doi.org/10.1038/353031a0
  8. Bowman JL, Smyth DR, Meyerowitz EM. Genes directing flower development in Arabidopsis. Plant Cell 1989;1:37-52.
  9. Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, et al. The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 1995;7:1859-1868.
  10. Ma C, Yang J, Cheng Q, Mao A, Zhang J, Wang S, et al. Comparative analysis of miRNA and mRNA abundance in determinate cucumber by high-throughput sequencing. PLoS One 2018;13:e0190691.
  11. Gramzow L, Theissen G. A hitchhiker's guide to the MADS world of plants. Genome Biol 2010;11:214.
  12. Chanderbali AS, Berger BA, Howarth DG, Soltis PS, Soltis DE. Evolving ideas on the origin and evolution of flowers: new perspectives in the genomic era. Genetics 2016;202:1255-1265. https://doi.org/10.1534/genetics.115.182964
  13. Matsunaga S, Isono E, Kejnovsky E, Vyskot B, Dolezel J, Kawano S, et al. Duplicative transfer of a MADS box gene to a plant Y chromosome. Mol Biol Evol 2003;20:1062-1069. https://doi.org/10.1093/molbev/msg114
  14. Jack T, Brockman LL, Meyerowitz EM. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 1992;68:683-697. https://doi.org/10.1016/0092-8674(92)90144-2
  15. Sugiyama R, Kazama Y, Miyazawa Y, Matsunaga S, Kawano S. CCLS96.1, a member of a multicopy gene family, may encode a non-coding RNA preferentially transcribed in reproductive organs of Silene latifolia. DNA Res 2003;10:213-220. https://doi.org/10.1093/dnares/10.5.213
  16. Kejnovsky E, Hobza R, Cermak T, Kubat Z, Vyskot B. The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity (Edinb) 2009;102:533-541. https://doi.org/10.1038/hdy.2009.17
  17. Matsunaga S. Sex chromosome-linked genes in plants. Genes Genet Syst 2006;81:219-226. https://doi.org/10.1266/ggs.81.219
  18. Stewart D, Graciet E, Wellmer F. Molecular and regulatory mechanisms controlling floral organ development. FEBS J 2016;283:1823-1830. https://doi.org/10.1111/febs.13640
  19. Smaczniak C, Immink RG, Angenent GC, Kaufmann K. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 2012;139:3081-3098. https://doi.org/10.1242/dev.074674
  20. Theissen G, Melzer R, Rumpler F. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 2016;143:3259-3271. https://doi.org/10.1242/dev.134080
  21. Masiero S, Colombo L, Grini PE, Schnittger A, Kater MM. The emerging importance of type I MADS box transcription factors for plant reproduction. Plant Cell 2011;23:865-872. https://doi.org/10.1105/tpc.110.081737
  22. Becker A, Theissen G. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 2003;29:464-489. https://doi.org/10.1016/S1055-7903(03)00207-0
  23. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A 2008;105:16831-16836. https://doi.org/10.1073/pnas.0808687105
  24. Tapia-Lopez R, Garcia-Ponce B, Dubrovsky JG, Garay-Arroyo A, Perez-Ruiz RV, Kim SH, et al. An AGAMOUS-related MADS-box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis. Plant Physiol 2008;146:1182-1192. https://doi.org/10.1104/pp.107.108647
  25. Heijmans K, Morel P, Vandenbussche M. MADS-box genes and floral development: the dark side. J Exp Bot 2012;63:5397-5404. https://doi.org/10.1093/jxb/ers233
  26. Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, et al. Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 2008;135:1481-1491. https://doi.org/10.1242/dev.020255
  27. Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat Genet 2008;40:1489-1492. https://doi.org/10.1038/ng.253
  28. Li C, Wang Y, Xu L, Nie S, Chen Y, Liang D, et al. Genome-wide characterization of the MADS-box gene family in radish (Raphanus sativus L.) and assessment of its roles in flowering and floral organogenesis. Front Plant Sci 2016;7:1390.
  29. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, et al. A transposon-induced epigenetic change leads to sex determination in melon. Nature 2009;461:1135-1138. https://doi.org/10.1038/nature08498
  30. Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, et al. Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 2009;5:e1000440.
  31. Mandaokar A, Browse J. MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol 2009;149:851-862. https://doi.org/10.1104/pp.108.132597
  32. Millar AA, Gubler F. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 2005;17:705-721. https://doi.org/10.1105/tpc.104.027920
  33. Wang X, Niu QW, Teng C, Li C, Mu J, Chua NH, et al. Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res 2009;19:224-235. https://doi.org/10.1038/cr.2008.276
  34. Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D. A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 2009;5:e1000430.
  35. Lee DK, Geisler M, Springer PS. LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 2009;136:2423-2432. https://doi.org/10.1242/dev.031971
  36. Murase K, Shigenobu S, Fujii S, Ueda K, Murata T, Sakamoto A, et al. MYB transcription factor gene involved in sex determination in Asparagus officinalis. Genes Cells 2017;22:115-123. https://doi.org/10.1111/gtc.12453
  37. Samad AF, Sajad M, Nazaruddin N, Fauzi IA, Murad AM, Zainal Z, et al. MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 2017;8:565.
  38. Akagi T, Henry IM, Tao R, Comai L. Plant genetics. A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science 2014;346:646-650. https://doi.org/10.1126/science.1257225
  39. Fornara F, de Montaigu A, Coupland G. SnapShot: control of flowering in Arabidopsis. Cell 2010;141:550.
  40. Wu T, Qin Z, Zhou X, Feng Z, Du Y. Transcriptome profile analysis of floral sex determination in cucumber. J Plant Physiol 2010;167:905-913. https://doi.org/10.1016/j.jplph.2010.02.004
  41. Yoo MJ, Chanderbali AS, Altman NS, Soltis PS, Soltis DE. Evolutionary trends in the floral transcriptome: insights from one of the basalmost angiosperms, the water lily Nuphar advena (Nymphaeaceae). Plant J 2010;64:687-698. https://doi.org/10.1111/j.1365-313X.2010.04357.x
  42. Zahn LM, Ma X, Altman NS, Zhang Q, Wall PK, Tian D, et al. Comparative transcriptomics among floral organs of the basal eudicot Eschscholzia californica as reference for floral evolutionary developmental studies. Genome Biol 2010;11:R101.
  43. Zhang XM, Zhao L, Larson-Rabin Z, Li DZ, Guo ZH. De novo sequencing and characterization of the floral transcriptome of Dendrocalamus latiflorus (Poaceae: Bambusoideae). PLoS One 2012;7:e42082.
  44. Logacheva MD, Kasianov AS, Vinogradov DV, Samigullin TH, Gelfand MS, Makeev VJ, et al. De novo sequencing and characterization of floral transcriptome in two species of buckwheat (Fagopyrum). BMC Genomics 2011;12:30.
  45. Varkonyi-Gasic E, Moss SM, Voogd C, Wu R, Lough RH, Wang YY, et al. Identification and characterization of flowering genes in kiwifruit: sequence conservation and role in kiwifruit flower development. BMC Plant Biol 2011;11:72.
  46. DeLong A, Calderon-Urrea A, Dellaporta SL. Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 1993;74:757-768. https://doi.org/10.1016/0092-8674(93)90522-R
  47. Boualem A, Fergany M, Fernandez R, Troadec C, Martin A, Morin H, et al. A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 2008;321:836-838. https://doi.org/10.1126/science.1159023
  48. Charlesworth D, Mank JE. The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 2010;186:9-31. https://doi.org/10.1534/genetics.110.117697
  49. Renner SS. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 2014;101:1588-1596. https://doi.org/10.3732/ajb.1400196
  50. Cho J, Koo DH, Nam YW, Han CT, Lim HT, Bang JW, et al. Isolation and characterization of cDNA clones expressed under male sex expression conditions in a monoecious cucumber plant (Cucumis sativus L. cv. Winter Long). Euphytica 2005;146:271-281. https://doi.org/10.1007/s10681-005-9023-1
  51. Gao WJ, Li SF, Zhang GJ, Wang NN, Deng CL, Lu LD. Comparative analysis of gene expression by microarray analysis of male and female flowers of Asparagus officinalis. Biosci Biotechnol Biochem 2013;77:1193-1199. https://doi.org/10.1271/bbb.120943
  52. Garber M, Grabherr MG, Guttman M, Trapnell C. Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 2011;8:469-477. https://doi.org/10.1038/nmeth.1613
  53. Xiao M, Zhang Y, Chen X, Lee EJ, Barber CJ, Chakrabarty R, et al. Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. J Biotechnol 2013;166:122-134. https://doi.org/10.1016/j.jbiotec.2013.04.004
  54. Guo S, Zheng Y, Joung JG, Liu S, Zhang Z, Crasta OR, et al. Transcriptome sequencing and comparative analysis of cucumber flowers with different sex types. BMC Genomics 2010;11:384.
  55. Rhee SJ, Seo M, Jang YJ, Cho S, Lee GP. Transcriptome profiling of differentially expressed genes in floral buds and flowers of male sterile and fertile lines in watermelon. BMC Genomics 2015;16:914.
  56. Yan X, Dong C, Yu J, Liu W, Jiang C, Liu J, et al. Transcriptome profile analysis of young floral buds of fertile and sterile plants from the self-pollinated offspring of the hybrid between novel restorer line NR1 and Nsa CMS line in Brassica napus. BMC Genomics 2013;14:26.
  57. Rocheta M, Sobral R, Magalhaes J, Amorim MI, Ribeiro T, Pinheiro M, et al. Comparative transcriptomic analysis of male and female flowers of monoecious Quercus suber. Front Plant Sci 2014;5:599.
  58. Allen RL, Lonsdale DM. Molecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development. Plant J 1993;3:261-271. https://doi.org/10.1111/j.1365-313X.1993.tb00177.x
  59. Tebbutt SJ, Rogers HJ, Lonsdale DM. Characterization of a tobacco gene encoding a pollen-specific polygalacturonase. Plant Mol Biol 1994;25:283-297. https://doi.org/10.1007/BF00023244
  60. Rhee SY, Osborne E, Poindexter PD, Somerville CR. Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 2003;133:1170-1180. https://doi.org/10.1104/pp.103.028266
  61. Ogawa M, Kay P, Wilson S, Swain SM. ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are Polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 2009;21:216-233. https://doi.org/10.1105/tpc.108.063768
  62. Yu L, Sun J, Li L. PtrCel9A6, an endo-1,4-beta-glucanase, is required for cell wall formation during xylem differentiation in populus. Mol Plant 2013;6:1904-1917. https://doi.org/10.1093/mp/sst104
  63. Liu K, Feng S, Pan Y, Zhong J, Chen Y, Yuan C, et al. Transcriptome analysis and identification of genes associated with floral transition and flower development in sugar apple (Annona squamosa L.). Front Plant Sci 2016;7:1695.
  64. Liu J, Yin T, Ye N, Chen Y, Yin T, Liu M, et al. Transcriptome analysis of the differentially expressed genes in the male and female shrub willows (Salix suchowensis). PLoS One 2013;8:e60181.
  65. Alagna F, Cirilli M, Galla G, Carbone F, Daddiego L, Facella P, et al. Transcript analysis and regulative events during flower development in olive (Olea europaea L.). PLoS One 2016;11:e0152 943.
  66. Du S, Sang Y, Liu X, Xing S, Li J, Tang H, et al. Transcriptome profile analysis from different sex types of Ginkgo biloba L. Front Plant Sci 2016;7:871.
  67. Shi T, Gao Z, Wang L, Zhang Z, Zhuang W, Sun H, et al. Identification of differentially-expressed genes associated with pistil abortion in Japanese apricot by genome-wide transcriptional analysis. PLoS One 2012;7:e47810.
  68. Fan L, Chen M, Dong B, Wang N, Yu Q, Wang X, et al. Transcriptomic analysis of flower bud differentiation in Magnolia sinostellata. Genes (Basel) 2018;9:212.