The Evolution of Spinnable Cotton Fiber Entailed Prolonged Development and a Novel Metabolism
A central question in evolutionary biology concerns the developmental processes by which new phenotypes arise. An exceptional example of evolutionary innovation is the single-celled seed trichome in Gossypium (“cotton fiber”). We have used fiber development in Gossypium as a system to understand how morphology can rapidly evolve. Fiber has undergone considerable morphological changes between the short, tightly adherent fibers of G. longicalyx and the derived long, spinnable fibers of its closest relative, G. herbaceum, which facilitated cotton domestication. We conducted comparative gene expression profiling across a developmental time-course of fibers from G. longicalyx and G. herbaceum using microarrays with ∼22,000 genes. Expression changes between stages were temporally protracted in G. herbaceum relative to G. longicalyx, reflecting a prolongation of the ancestral developmental program. Gene expression and GO analyses showed that many genes involved with stress responses were upregulated early in G. longicalyx fiber development. Several candidate genes upregulated in G. herbaceum have been implicated in regulating redox levels and cell elongation processes. Three genes previously shown to modulate hydrogen peroxide levels were consistently expressed in domesticated and wild cotton species with long fibers, but expression was not detected by quantitative real time-PCR in wild species with short fibers. Hydrogen peroxide is important for cell elongation, but at high concentrations it becomes toxic, activating stress processes that may lead to early onset of secondary cell wall synthesis and the end of cell elongation. These observations suggest that the evolution of long spinnable fibers in cotton was accompanied by novel expression of genes assisting in the regulation of reactive oxygen species levels. Our data suggest a model for the evolutionary origin of a novel morphology through differential gene regulation causing prolongation of an ancestral developmental program.
Vyšlo v časopise:
The Evolution of Spinnable Cotton Fiber Entailed Prolonged Development and a Novel Metabolism. PLoS Genet 4(2): e25. doi:10.1371/journal.pgen.0040025
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.0040025
Souhrn
A central question in evolutionary biology concerns the developmental processes by which new phenotypes arise. An exceptional example of evolutionary innovation is the single-celled seed trichome in Gossypium (“cotton fiber”). We have used fiber development in Gossypium as a system to understand how morphology can rapidly evolve. Fiber has undergone considerable morphological changes between the short, tightly adherent fibers of G. longicalyx and the derived long, spinnable fibers of its closest relative, G. herbaceum, which facilitated cotton domestication. We conducted comparative gene expression profiling across a developmental time-course of fibers from G. longicalyx and G. herbaceum using microarrays with ∼22,000 genes. Expression changes between stages were temporally protracted in G. herbaceum relative to G. longicalyx, reflecting a prolongation of the ancestral developmental program. Gene expression and GO analyses showed that many genes involved with stress responses were upregulated early in G. longicalyx fiber development. Several candidate genes upregulated in G. herbaceum have been implicated in regulating redox levels and cell elongation processes. Three genes previously shown to modulate hydrogen peroxide levels were consistently expressed in domesticated and wild cotton species with long fibers, but expression was not detected by quantitative real time-PCR in wild species with short fibers. Hydrogen peroxide is important for cell elongation, but at high concentrations it becomes toxic, activating stress processes that may lead to early onset of secondary cell wall synthesis and the end of cell elongation. These observations suggest that the evolution of long spinnable fibers in cotton was accompanied by novel expression of genes assisting in the regulation of reactive oxygen species levels. Our data suggest a model for the evolutionary origin of a novel morphology through differential gene regulation causing prolongation of an ancestral developmental program.
Zdroje
1. DoebleyJStecAHubbardL
1997
The evolution of apical dominance in maize.
Nature
386
485
488
2. WangHNussbaum-WaglerTLiBZhaoQVigourouxY
2005
The origin of the naked grains of maize.
Nature
436
714
719
3. LiCBZhouALSangT
2006
Rice domestication by reducing shattering.
Science
311
1936
1939
4. KonishiSIzawaTLinSYEbanaKFukutaY
2006
An SNP caused loss of seed shattering during rice domestication.
Science
312
1392
1396
5. FraryANesbittTCFraryAGrandilloSvan der KnaapE
2000
fw2.2: A quantitative trait locus key to the evolution of tomato fruit size.
Science
289
85
88
6. SimonsKJFellersJPTrickHNZhangZCTaiYS
2006
Molecular characterization of the major wheat domestication gene Q.
Genetics
172
547
555
7. DoebleyJ
2006
Unfallen grains: how ancient farmers turned weeds into crops.
Science
312
1318
1319
8. KimHJTriplettBA
2001
Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis.
Plant Physiol
127
1361
1366
9. BrubakerCLBourlandFMWendelJF
1999
The origin and domestication of cotton.
SmithCWCothrenJT
In:
Cotton: origin, history, technology and production
New York
John Wiley and Sons
3
31
10. WendelJF
1995
Cotton.
In:
SimmondsNSmarttJ
Evolution of crop plants
London
Longman
358
366
11. WendelJFCronnRC
2002
Polyploidy and the evolutionary history of cotton.
Adv Agron
78
159
186
12. WendelJFAlbertVA
1992
Phylogenetics of the cotton genus (Gossypium)-character-state weighted parsimony analysis of chloroplast-DNA restriction site data and its systematic and biogeographic implications.
Syst Bot
17
115
143
13. SeelananTSchnabelAWendelJF
1997
Congruence and consensus in the cotton tribe (Malvaceae).
Syst Bot
22
259
290
14. DillehayTDRossenJAndresTCWilliamsDE
2007
Preceramic adoption of peanut, squash, and cotton in northern Peru.
Science
316
1890
1893
15. ApplequistWLCronnRWendelJF
2001
Comparative development of fiber in wild and cultivated cotton.
Evol Dev
3
3
17
16. NaithaniSCRama RaoNSinghYD
1982
Physiological and biochemical changes associated with cotton fibre development.
Physiol Plantarum
54
225
229
17. BeasleyCA
1979
Cellulose content in fibers of cottons which differ in their lint lengths and extent of fuzz.
Physiol Plantarum
45
77
82
18. MeinertMCDelmerDP
1977
Changes in biochemical composition of the cell wall of the cotton fiber during development.
Plant Physiol
59
1088
1097
19. HutchJBLeeBJS
1958
Notes from the East African Herbarium: IX. A new species of Gossypium from central Tan-ganyika.
Kew Bull
13
221
223
20. UdallJAFlagelLECheungFWoodwardAWHovavR
2007
Spotted cotton oligonucleotide microarrays for gene expression analysis.
BMC Genomics
8
81
21. HovavRUdallJAHovavERappRAFlagelL
2007
A majority of genes are expressed in the single-celled seed trichome of cotton.
Planta
227
319
329
22. RodriguezAAGrunbergKATaleisnikEL
2002
Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension.
Plant Physiol
129
1627
1632
23. ForemanJDemidchikVBothwellJHFMylonaPMiedemaH
2003
Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.
Nature
422
442
446
24. FrySC
1998
Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals.
Biochemical J
332
507
515
25. LiszkayAvan der ZalmESchopferP
2004
Production of reactive oxygen intermediates (O2˙—, H2O2, and ˙OH) by maize roots and their role in wall loosening and elongation growth.
Plant Physiol
136
3114
3123
26. SchopferP
1996
Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles.
Planta
199
43
49
27. WigodaNBen-NissanGGranotDSchwartzAWeissD
2006
The gibberellin-induced, cysteine-rich protein GIP2 from Petunia hybrida exhibits in planta antioxidant activity.
Plant J
48
796
805
28. YangSHYangHJGrisafiPSanchatjateSFinkGR
2006
The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis.
Plant J
45
166
179
29. Lopez-HuertasECharltonWLJohnsonBGrahamIABakerA
2000
Stress induces peroxisome biogenesis genes.
EMBO J
19
6770
6777
30. ArpatABWaughMSullivanJPGonzalesMFrischD
2004
Functional genomics of cell elongation in developing cotton fibers.
Plant Mol Biol
54
911
929
31. ShiYHZhuSWMaoXZFengJXQinYM
2006
Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation.
Plant Cell
18
651
664
32. TaliercioEWBoykinD
2007
Analysis of gene expression in cotton fiber initials.
BMC Plant Biol
7
22
33. WuYLiewellynDJWhiteRRuggieroKAl-GhaziY
2007
Laser capture microdissection and cDNA microarrays used to generate gene expression profiles of rapidly expanding fibre initials cells on surface of cotton ovules.
Planta
226
1475
1490
34. CosgroveDJ
1999
Enzymes and other agents that enhance cell wall extensibility.
Annual Rev Plant Physiol Plant Mol Biol
50
391
417
35. PotikhaTSCollinsCCJohnsonDIDelmerDPLevineA
1999
The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers.
Plant Physiol
119
849
858
36. LiHBQinYMPangYSongWQMeiWQ
2007
A cotton ascorbate peroxidase is involved in hydrogen peroxide homeostasis during fibre cell development.
New Phytol
175
462
471
37. ShiLFOlszewskiNE
1998
Gibberellin and abscisic acid regulate GAST1 expression at the level of transcription.
Plant Mol Biol
38
1053
1060
38. Ben-NissanGLeeJYBorohovAWeissD
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
39. HuaJGrisafiPChengSHFinkGR
2001
Plant growth homeostasis is controlled by the Arabidopsis BON1 and BAP1 genes.
Genes Dev
15
2263
2272
40. JambunathanNSianiJMMcNellisTW
2001
A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance.
Plant Cell
13
2225
2240
41. FaberKNHeymanJASubramaniS
1998
Two AAA family peroxins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes.
Mol Cell Biol
18
936
943
42. KielJHilbrandsREVan der KleiIJRasmussenSWSalomonsFA
1999
Hansenula polymorpha Pex1p and Pex6p are peroxisome-associated AAA proteins that functionally and physically interact.
Yeast
15
1059
1078
43. FryxellPA
1979
The natural history of the cotton tribe
College Station (Texas)
Texas A&M University Press
44. WilkinsTASmartLB
1996
Isolation of RNA from plant tissue.
In:
PaK
A laboratory guide to RNA isolation, analysis, and synthesis
New York
Wiley-Liss
21
41
45. StoreyJDTibshiraniR
2003
SAM thresholding and false discovery rates for detecting differential gene expression in DNA microarrays.
In:
ParmigianiGGarrettESIrizarryRAZegerSL
The analysis of gene expression data: methods and software
New York
Springer
272
290
46. BluthgenNBrandKCajavecBSwatMHerzelH
2005
Biological profiling of gene groups utilizing Gene Ontology.
Genome Inform Ser Workshop Genome Inform
16
106
115
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2008 Číslo 2
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