Comparative Evolutionary and Developmental Dynamics of the Cotton () Fiber Transcriptome
The single-celled cotton (Gossypium hirsutum) fiber provides an excellent model to investigate how human selection affects phenotypic evolution. To gain insight into the evolutionary genomics of cotton domestication, we conducted comparative transcriptome profiling of developing cotton fibers using RNA-Seq. Analysis of single-celled fiber transcriptomes from four wild and five domesticated accessions from two developmental time points revealed that at least one-third and likely one-half of the genes in the genome are expressed at any one stage during cotton fiber development. Among these, ∼5,000 genes are differentially expressed during primary and secondary cell wall synthesis between wild and domesticated cottons, with a biased distribution among chromosomes. Transcriptome data implicate a number of biological processes affected by human selection, and suggest that the domestication process has prolonged the duration of fiber elongation in modern cultivated forms. Functional analysis suggested that wild cottons allocate greater resources to stress response pathways, while domestication led to reprogrammed resource allocation toward increased fiber growth, possibly through modulating stress-response networks. This first global transcriptomic analysis using multiple accessions of wild and domesticated cottons is an important step toward a more comprehensive systems perspective on cotton fiber evolution. The understanding that human selection over the past 5,000+ years has dramatically re-wired the cotton fiber transcriptome sets the stage for a deeper understanding of the genetic architecture underlying cotton fiber synthesis and phenotypic evolution.
Vyšlo v časopise:
Comparative Evolutionary and Developmental Dynamics of the Cotton () Fiber Transcriptome. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004073
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004073
Souhrn
The single-celled cotton (Gossypium hirsutum) fiber provides an excellent model to investigate how human selection affects phenotypic evolution. To gain insight into the evolutionary genomics of cotton domestication, we conducted comparative transcriptome profiling of developing cotton fibers using RNA-Seq. Analysis of single-celled fiber transcriptomes from four wild and five domesticated accessions from two developmental time points revealed that at least one-third and likely one-half of the genes in the genome are expressed at any one stage during cotton fiber development. Among these, ∼5,000 genes are differentially expressed during primary and secondary cell wall synthesis between wild and domesticated cottons, with a biased distribution among chromosomes. Transcriptome data implicate a number of biological processes affected by human selection, and suggest that the domestication process has prolonged the duration of fiber elongation in modern cultivated forms. Functional analysis suggested that wild cottons allocate greater resources to stress response pathways, while domestication led to reprogrammed resource allocation toward increased fiber growth, possibly through modulating stress-response networks. This first global transcriptomic analysis using multiple accessions of wild and domesticated cottons is an important step toward a more comprehensive systems perspective on cotton fiber evolution. The understanding that human selection over the past 5,000+ years has dramatically re-wired the cotton fiber transcriptome sets the stage for a deeper understanding of the genetic architecture underlying cotton fiber synthesis and phenotypic evolution.
Zdroje
1. OlsenKM, WendelJF (2013) A bountiful harvest: genomic insights into crop domestication phenotypes. Annu Rev Plant Biol 64: 47–70.
2. OlsenKM, WendelJF (2013) Crop plants as models for understanding plant adaptation and diversification. Front Plant Sci 4: 290.
3. DoebleyJF, GautBS, SmithBD (2006) The molecular genetics of crop domestication. Cell 127: 1309–1321.
4. Wendel JF, Flagel L, Adams KL (2012) Jeans, genes, and genomes: cotton as a model for studying polyploidy. In: Soltis PS, Soltis DE, editors. Polyploidy and Genome Evolution. Berlin: Springer. pp. 181–207.
5. WendelJF, CronnRC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78: 139–186.
6. JiaoY, WickettNJ, AyyampalayamS, ChanderbaliAS, LandherrL, et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100.
7. BaoY, HuG, FlagelLE, SalmonA, BezanillaM, et al. (2011) Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium). Proc Natl Acad Sci U S A 108: 21152–21157.
8. UdallJA, SwansonJM, HallerK, RappRA, SparksME, et al. (2006) A global assembly of cotton ESTs. Genome Res 16: 441–450.
9. LacapeJM, ClaverieM, VidalRO, CarazzolleMF, Guimaraes PereiraGA, et al. (2012) Deep sequencing reveals differences in the transcriptional landscapes of fibers from two cultivated species of cotton. PLoS One 7: e48855.
10. HinchliffeDJ, TurleyRB, NaoumkinaM, KimHJ, TangY, et al. (2011) A combined functional and structural genomics approach identified an EST-SSR marker with complete linkage to the Ligon lintless-2 genetic locus in cotton (Gossypium hirsutum L.). BMC Genomics 12: 445.
11. LiuK, SunJ, YaoL, YuanY (2012) Transcriptome analysis reveals critical genes and key pathways for early cotton fiber elongation in Ligon lintless-1 mutant. Genomics 100: 42–50.
12. NaoumkinaM, HinchliffeDJ, TurleyRB, BlandJM, FangDD (2013) Integrated metabolomics and genomics analysis provides new insights into the fiber elongation process in Ligon lintless-2 mutant cotton (Gossypium hirsutum L.). BMC Genomics 14: 155.
13. RappRA, HaiglerCH, FlagelL, HovavRH, UdallJA, et al. (2010) Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication. BMC Biol 8: 139.
14. WuY, MachadoAC, WhiteRG, LlewellynDJ, DennisES (2006) Expression profiling identifies genes expressed early during lint fibre initiation in cotton. Plant Cell Physiol 47: 107–127.
15. WangZ, GersteinM, SnyderM (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57–63.
16. PatersonAH, WendelJF, GundlachH, GuoH, JenkinsJ, et al. (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492: 423–427.
17. KimHJ, TriplettBA (2001) Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol 127: 1361–1366.
18. HaiglerCH, BetancurL, StiffMR, TuttleJR (2012) Cotton fiber: a powerful single-cell model for cell wall and cellulose research. Front Plant Sci 3: 104.
19. MarioniJC, MasonCE, ManeSM, StephensM, GiladY (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509–1517.
20. HovavR, UdallJA, HovavE, RappR, FlagelL, et al. (2008) A majority of cotton genes are expressed in single-celled fiber. Planta 227: 319–329.
21. ArpatAB, WaughM, SullivanJP, GonzalesM, FrischD, et al. (2004) Functional genomics of cell elongation in developing cotton fibers. Plant Mol Biol 54: 911–929.
22. ChaudharyB, HovavR, RappR, VermaN, UdallJA, et al. (2008) Global analysis of gene expression in cotton fibers from wild and domesticated Gossypium barbadense. Evol Dev 10: 567–582.
23. BetancurL, SinghB, RappRA, WendelJF, MarksMD, et al. (2010) Phylogenetically distinct cellulose synthase genes support secondary wall thickening in arabidopsis shoot trichomes and cotton fiber. J Integr Plant Biol 52: 205–220.
24. LiepmanAH, CavalierDM (2012) The CELLULOSE SYNTHASE-LIKE A and CELLULOSE SYNTHASE-LIKE C families: recent advances and future perspectives. Front Plant Sci 3: 109.
25. CarpitaNC (2011) Update on mechanisms of plant cell wall biosynthesis: how plants make cellulose and other (1->4)-beta-D-glycans. Plant Physiol 155: 171–184.
26. FarrokhiN, BurtonRA, BrownfieldL, HrmovaM, WilsonSM, et al. (2006) Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 4: 145–167.
27. LerouxelO, CavalierDM, LiepmanAH, KeegstraK (2006) Biosynthesis of plant cell wall polysaccharides - a complex process. Curr Opin Plant Biol 9: 621–630.
28. Stiff MR, Haigler CH (2012) Recent advances in cotton fiber development. In: Oosterhuis DM, Cothren JT, editors. Flowering and fruiting in cotton. Tennessee: The Cotton Foundation. pp. 163–192.
29. JiSJ, LuYC, FengJX, WeiG, LiJ, et al. (2003) Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic acids research 31: 2534–2543.
30. QinYM, PujolFM, HuCY, FengJX, KastaniotisAJ, et al. (2007) Genetic and biochemical studies in yeast reveal that the cotton fibre-specific GhCER6 gene functions in fatty acid elongation. J Exp Bot 58: 473–481.
31. QinYM, HuCY, PangY, KastaniotisAJ, HiltunenJK, et al. (2007) Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant cell 19: 3692–3704.
32. MacMillanCP, MansfieldSD, StachurskiZH, EvansR, SouthertonSG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J 62: 689–703.
33. ShiH, KimY, GuoY, StevensonB, ZhuJK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant cell 15: 19–32.
34. HuangGQ, GongSY, XuWL, LiW, LiP, et al. (2013) A fasciclin-like arabinogalactan protein, GhFLA1, is involved in fiber initiation and elongation of cotton. Plant Physiol 161: 1278–1290.
35. ArgiriouA, KalivasA, MichailidisG, TsaftarisA (2012) Characterization of PROFILIN genes from allotetraploid (Gossypium hirsutum) cotton and its diploid progenitors and expression analysis in cotton genotypes differing in fiber characteristics. Mol Biol Rep 39: 3523–3532.
36. McKinneyEC, MeagherRB (1998) Members of the Arabidopsis actin gene family are widely dispersed in the genome. Genetics 149: 663–675.
37. GillilandLU, PawloskiLC, KandasamyMK, MeagherRB (2003) Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. Plant J 33: 319–328.
38. McDowellJM, AnYQ, HuangS, McKinneyEC, MeagherRB (1996) The arabidopsis ACT7 actin gene is expressed in rapidly developing tissues and responds to several external stimuli. Plant physiology 111: 699–711.
39. KandasamyMK, McKinneyEC, MeagherRB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant cell 21: 701–718.
40. LiXB, FanXP, WangXL, CaiL, YangWC (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant cell 17: 859–875.
41. Tominaga-WadaR, IwataM, SugiyamaJ, KotakeT, IshidaT, et al. (2009) The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. Plant J 60: 564–574.
42. GalbiatiM, MatusJT, FranciaP, RusconiF, CanonP, et al. (2011) The grapevine guard cell-related VvMYB60 transcription factor is involved in the regulation of stomatal activity and is differentially expressed in response to ABA and osmotic stress. BMC Plant Biol 11: 142.
43. OhJE, KwonY, KimJH, NohH, HongSW, et al. (2011) A dual role for MYB60 in stomatal regulation and root growth of Arabidopsis thaliana under drought stress. Plant Mol Biol 77: 91–103.
44. ParkJS, KimJB, ChoKJ, CheonCI, SungMK, et al. (2008) Arabidopsis R2R3-MYB transcription factor AtMYB60 functions as a transcriptional repressor of anthocyanin biosynthesis in lettuce (Lactuca sativa). Plant Cell Rep 27: 985–994.
45. MachadoA, WuY, YangY, LlewellynDJ, DennisES (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J 59: 52–62.
46. WalfordSA, WuY, LlewellynDJ, DennisES (2011) GhMYB25-like: a key factor in early cotton fibre development. Plant J 65: 785–797.
47. PuL, LiQ, FanX, YangW, XueY (2008) The R2R3 MYB transcription factor GhMYB109 is required for cotton fiber development. Genetics 180: 811–820.
48. SuoJ, LiangX, PuL, ZhangY, XueY (2003) Identification of GhMYB109 encoding a R2R3 MYB transcription factor that expressed specifically in fiber initials and elongating fibers of cotton (Gossypium hirsutum L.). Biochim Biophys Acta 1630: 25–34.
49. HaoJ, TuL, HuH, TanJ, DengF, et al. (2012) GbTCP, a cotton TCP transcription factor, confers fibre elongation and root hair development by a complex regulating system. J Exp Bot 63: 6267–6281.
50. WangMY, ZhaoPM, ChengHQ, HanLB, WuXM, et al. (2013) The Cotton transcription factor TCP14 functions in auxin-mediated epidermal cell differentiation and elongation. Plant Physiol 162: 1669–1680.
51. XiaoYH, LiDM, YinMH, LiXB, ZhangM, et al. (2010) Gibberellin 20-oxidase promotes initiation and elongation of cotton fibers by regulating gibberellin synthesis. J Plant Physiol 167: 829–837.
52. BeasleyCA, TingIP (1974) The effects of plant growth substances on in vitro fiber development from unfertilized cotton ovules. Am J Bot 61: 188–194.
53. WanjieSW, WeltiR, MoreauRA, ChapmanKD (2005) Identification and quantification of glycerolipids in cotton fibers: reconciliation with metabolic pathway predictions from DNA databases. Lipids 40: 773–785.
54. GroverCE, GallagherJP, SzadkowskiEP, YooMJ, FlagelLE, et al. (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196: 966–971.
55. YooMJ, SzadkowskiE, WendelJF (2013) Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110: 171–180.
56. ApplequistWL, CronnR, WendelJF (2001) Comparative development of fiber in wild and cultivated cotton. Evol Dev 3: 3–17.
57. SeagullRW, OliveriV, MurphyK, BinderA, KothariS (2000) Cotton fiber growth and development 2. Changes in cell diameter and wall birefringence. J Cotton Sci 4: 97–104.
58. HovavR, UdallJA, ChaudharyB, HovavE, FlagelL, et al. (2008) The evolution of spinnable cotton fiber entailed prolonged development and a novel metabolism. PLoS Genet 4: e25.
59. HuG, KohJ, YooMJ, GruppK, ChenS, et al. (2013) Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytol 200: 570–582.
60. RubinovichL, WeissD (2010) The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. Plant J 64: 1018–1027.
61. HundertmarkM, HinchaDK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9: 118.
62. SeoPJ, ParkJM, KangSK, KimSG, ParkCM (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233: 189–200.
63. HsiehTH, LiCW, SuRC, ChengCP, Sanjaya, et al. (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231: 1459–1473.
64. TanJ, TuL, DengF, HuH, NieY, et al. (2013) A genetic and metabolic analysis revealed that cotton fiber cell development was retarded by flavonoid naringenin. Plant Physiol 162: 86–95.
65. FengH, TianX, LiuY, LiY, ZhangX, et al. (2013) Analysis of flavonoids and the flavonoid structural genes in brown fiber of upland cotton. PLoS One 8: e58820.
66. RambaniA, PageJT, UdallJA (2013) Polyploidy and the petal transcriptome of Gossypium. BMC Plant Biol (in press).
67. PadmalathaKV, DhandapaniG, KanakachariM, KumarS, DassA, et al. (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Mol Biol 78: 223–246.
68. WangCY, ChiouCY, WangHL, KrishnamurthyR, VenkatagiriS, et al. (2008) Carbohydrate mobilization and gene regulatory profile in the pseudobulb of Oncidium orchid during the flowering process. Planta 227: 1063–1077.
69. BabbVM, HaiglerCH (2001) Sucrose phosphate synthase activity rises in correlation with high-rate cellulose synthesis in three heterotrophic systems. Plant Physiol 127: 1234–1242.
70. PadmalathaKV, PatilDP, KumarK, DhandapaniG, KanakachariM, et al. (2012) Functional genomics of fuzzless-lintless mutant of Gossypium hirsutum L. cv. MCU5 reveal key genes and pathways involved in cotton fibre initiation and elongation. BMC Genomics 13: 624.
71. LassnerMW, LardizabalK, MetzJG (1996) A jojoba beta-Ketoacyl-CoA synthase cDNA complements the canola fatty acid elongation mutation in transgenic plants. Plant cell 8: 281–292.
72. PourcelL, RoutaboulJM, CheynierV, LepiniecL, DebeaujonI (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12: 29–36.
73. Al-GhaziY, BourotS, ArioliT, DennisES, LlewellynDJ (2009) Transcript profiling during fiber development identifies pathways in secondary metabolism and cell wall structure that may contribute to cotton fiber quality. Plant Cell Physiol 50: 1364–1381.
74. ZhengZL (2009) Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav 4: 584–591.
75. NahirnakV, AlmasiaNI, HoppHE, Vazquez-RovereC (2012) Snakin/GASA proteins: involvement in hormone crosstalk and redox homeostasis. Plant Signal Behav 7: 1004–1008.
76. Ben-NissanG, WeissD (1996) The petunia homologue of tomato gast1: transcript accumulation coincides with gibberellin-induced corolla cell elongation. Plant Mol Biol 32: 1067–1074.
77. Ben-NissanG, LeeJY, BorohovA, WeissD (2004) GIP, a Petunia hybrida GA-induced cysteine-rich protein: a possible role in shoot elongation and transition to flowering. Plant J 37: 229–238.
78. KotilainenM, HelariuttaY, MehtoM, PollanenE, AlbertVA, et al. (1999) GEG participates in the regulation of cell and organ shape during corolla and carpel development in Gerbera hybrida. Plant cell 11: 1093–1104.
79. de la FuenteJI, AmayaI, CastillejoC, Sanchez-SevillaJF, QuesadaMA, et al. (2006) The strawberry gene FaGAST affects plant growth through inhibition of cell elongation. J Exp Bot 57: 2401–2411.
80. MittlerR, VanderauweraS, GolleryM, Van BreusegemF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490–498.
81. SharmaP, JhaAB, DubeyRS, PessarakliM (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 10.1155/2012/217037.
82. ChaudharyB, HovavR, FlagelL, MittlerR, WendelJF (2009) Parallel expression evolution of oxidative stress-related genes in fiber from wild and domesticated diploid and polyploid cotton (Gossypium). BMC Genomics 10: 378.
83. YangYW, BianSM, YaoY, LiuJY (2008) Comparative proteomic analysis provides new insights into the fiber elongating process in cotton. J Proteome Res 7: 4623–4637.
84. MeiW, QinY, SongW, LiJ, ZhuY (2009) Cotton GhPOX1 encoding plant class III peroxidase may be responsible for the high level of reactive oxygen species production that is related to cotton fiber elongation. J Genet Genomics 36: 141–150.
85. PotikhaTS, CollinsCC, JohnsonDI, DelmerDP, LevineA (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119: 849–858.
86. BrubakerCL, WendelJF (1994) Reevaluating the origin of domesticated cotton (Gossypium hirsutum: Malvaceae) using nuclear restriction fragment length polymorphisms (RFLPs). Am J Bot 81: 1309–1326.
87. Wilkins TA, Smart LB (1996) Isolation of RNA from plant tissue. In: Krieg PA, editor. A Laboratory Guide to RNA: solation, Analysis and Synthesis. New York: Wiley-Liss. pp. 21–41.
88. DoyleJJ, DoyleJL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15.
89. WuTD, NacuS (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873–881.
90. PageJT, GingleAR, UdallJA (2013) PolyCat: a resource for genome categorization of sequencing reads from allopolyploid organisms. G3 3: 517–525.
91. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.
92. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
93. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289–300.
94. ThompsonJD, HigginsDG, GibsonTJ (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: 4673–4680.
95. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
96. DuZ, ZhouX, LingY, ZhangZ, SuZ (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: W64–70.
97. BenjaminiY, YekutieliD (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29: 1165–1188.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 1
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- GATA6 Is a Crucial Regulator of Shh in the Limb Bud
- Large Inverted Duplications in the Human Genome Form via a Fold-Back Mechanism
- Down-Regulation of eIF4GII by miR-520c-3p Represses Diffuse Large B Cell Lymphoma Development
- Genome Sequencing Highlights the Dynamic Early History of Dogs