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Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication.

Rapp RA, Haigler CH, Flagel L, Hovav RH, Udall JA, Wendel JF - BMC Biol. (2010)

Bottom Line: About 15% of the differentially expressed genes in wild versus domesticated cotton fibre have no homology to the genes in databases.Gene expression during fibre development within accessions and expression alteration arising from evolutionary change appears to be 'modular' - complex genic networks have been simultaneously and similarly transformed, in a coordinated fashion, as a consequence of human-mediated selection.These results highlight the complex alteration of the global gene expression machinery that resulted from human selection for a longer, stronger and finer fibre, as well as other aspects of fibre physiology that were not consciously selected.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology, 251 Bessey Hall, Iowa State University, Ames, IA 50011, USA.

ABSTRACT

Background: Understanding the evolutionary genetics of modern crop phenotypes has a dual relevance to evolutionary biology and crop improvement. Modern upland cotton (Gossypium hirsutum L.) was developed following thousands of years of artificial selection from a wild form, G. hirsutum var. yucatanense, which bears a shorter, sparser, layer of single-celled, ovular trichomes ('fibre'). In order to gain an insight into the nature of the developmental genetic transformations that accompanied domestication and crop improvement, we studied the transcriptomes of cotton fibres from wild and domesticated accessions over a developmental time course.

Results: Fibre cells were harvested between 2 and 25 days post-anthesis and encompassed the primary and secondary wall synthesis stages. Using amplified messenger RNA and a custom microarray platform designed to interrogate expression for 40,430 genes, we determined global patterns of expression during fibre development. The fibre transcriptome of domesticated cotton is far more dynamic than that of wild cotton, with over twice as many genes being differentially expressed during development (12,626 versus 5273). Remarkably, a total of 9465 genes were diagnosed as differentially expressed between wild and domesticated fibres when summed across five key developmental time points. Human selection during the initial domestication and subsequent crop improvement has resulted in a biased upregulation of components of the transcriptional network that are important for agronomically advanced fibre, especially in the early stages of development. About 15% of the differentially expressed genes in wild versus domesticated cotton fibre have no homology to the genes in databases.

Conclusions: We show that artificial selection during crop domestication can radically alter the transcriptional developmental network of even a single-celled structure, affecting nearly a quarter of the genes in the genome. Gene expression during fibre development within accessions and expression alteration arising from evolutionary change appears to be 'modular' - complex genic networks have been simultaneously and similarly transformed, in a coordinated fashion, as a consequence of human-mediated selection. These results highlight the complex alteration of the global gene expression machinery that resulted from human selection for a longer, stronger and finer fibre, as well as other aspects of fibre physiology that were not consciously selected. We illustrate how the data can be mined for genes that were unwittingly targeted by aboriginal and/or modern domesticators during crop improvement and/or which potentially control the improved qualities of domesticated cotton fibre.See Commentary: http://www.biomedcentral.com/1741-7007/8/137.

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Genes differentially expressed during fibre development in cotton. Top row: domesticated TM-1. Bottom row: wild var. yucatanense. Green ellipses represent time points of RNA collection, from 2 to 25 days post anthesis (DPA). Arrows represent contrasts used in the statistical model. Numbers above or inside the arrows are the number of genes differentially diagnosed for the specified contrast. For example, for the two stages 2 and 7 DPA within domesticated G. hirsutum, 1988 genes were up-regulated at 2 DPA, whereas1545 were more highly expressed at 7 DPA. Contrasts are also shown between wild and domesticated G. hirsutum; for example between TM-1 and yucatanense at 2 DPA, 2904 genes were more highly expressed in the domesticated form, while for the same contrast 2133 are up-regulated in the wild cotton.
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Figure 3: Genes differentially expressed during fibre development in cotton. Top row: domesticated TM-1. Bottom row: wild var. yucatanense. Green ellipses represent time points of RNA collection, from 2 to 25 days post anthesis (DPA). Arrows represent contrasts used in the statistical model. Numbers above or inside the arrows are the number of genes differentially diagnosed for the specified contrast. For example, for the two stages 2 and 7 DPA within domesticated G. hirsutum, 1988 genes were up-regulated at 2 DPA, whereas1545 were more highly expressed at 7 DPA. Contrasts are also shown between wild and domesticated G. hirsutum; for example between TM-1 and yucatanense at 2 DPA, 2904 genes were more highly expressed in the domesticated form, while for the same contrast 2133 are up-regulated in the wild cotton.

Mentions: We explored the global transcriptional variation of 40,430 genes over a developmental time course of fibre differentiation (2, 7, 10, 20 and 25 DPA) in G. hirsutum cv. TM-1 (domesticated) versus var. yucatanense (wild). Figure 3 shows the number of unigenes up- and down-regulated at each stage. Overall, domesticated TM-1 displayed a much higher level of transcriptional variation between the sampled time points than did the wild yucatanense accession. When all the developmental transitions were included, 12,626 or 5273 genes experienced significant up- or down-regulation in domesticated or wild cotton, respectively (Figure 3). Between 2 and 7 DPA, 8.7% of assayed genes in TM-1 were differentially expressed [3533 unigenes; P-value ≤ 0.05; false discovery rate (FDR) ≤ 0.05], compared to 6.3% (2552 unigenes) in yucatanense. Notably, there was little change in the transcriptome between 7 and 10 DPA in TM-1, a period of active fibre elongation; only two unigenes were differentially expressed in TM-1, whereas 140 unigenes (0.35% of the total) had altered expression in yucatanense. This difference may relate to differences in the fibre elongation curves between 7 and 16 DPA; TM-1 was entering a sustained period of high rate elongation at 7 DPA whereas yucatanense elongation during this period is slower [5]. Far more genes showed altered expression between 10 DPA (during primary wall synthesis) and 20 DPA (when secondary wall thickening was beginning) in both genotypes (Figure 2) [24,25]. During this period, 18.8% (7575) and 6.2% (2516) of the unigenes were differentially expressed in TM-1 and in yucatanense, respectively. As secondary wall deposition continued between 20 to 25 DPA, only 1486 (3.7%) or 45 (0.1%) unigenes changed expression in TM-1 or yucatanense, respectively.


Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication.

Rapp RA, Haigler CH, Flagel L, Hovav RH, Udall JA, Wendel JF - BMC Biol. (2010)

Genes differentially expressed during fibre development in cotton. Top row: domesticated TM-1. Bottom row: wild var. yucatanense. Green ellipses represent time points of RNA collection, from 2 to 25 days post anthesis (DPA). Arrows represent contrasts used in the statistical model. Numbers above or inside the arrows are the number of genes differentially diagnosed for the specified contrast. For example, for the two stages 2 and 7 DPA within domesticated G. hirsutum, 1988 genes were up-regulated at 2 DPA, whereas1545 were more highly expressed at 7 DPA. Contrasts are also shown between wild and domesticated G. hirsutum; for example between TM-1 and yucatanense at 2 DPA, 2904 genes were more highly expressed in the domesticated form, while for the same contrast 2133 are up-regulated in the wild cotton.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2992495&req=5

Figure 3: Genes differentially expressed during fibre development in cotton. Top row: domesticated TM-1. Bottom row: wild var. yucatanense. Green ellipses represent time points of RNA collection, from 2 to 25 days post anthesis (DPA). Arrows represent contrasts used in the statistical model. Numbers above or inside the arrows are the number of genes differentially diagnosed for the specified contrast. For example, for the two stages 2 and 7 DPA within domesticated G. hirsutum, 1988 genes were up-regulated at 2 DPA, whereas1545 were more highly expressed at 7 DPA. Contrasts are also shown between wild and domesticated G. hirsutum; for example between TM-1 and yucatanense at 2 DPA, 2904 genes were more highly expressed in the domesticated form, while for the same contrast 2133 are up-regulated in the wild cotton.
Mentions: We explored the global transcriptional variation of 40,430 genes over a developmental time course of fibre differentiation (2, 7, 10, 20 and 25 DPA) in G. hirsutum cv. TM-1 (domesticated) versus var. yucatanense (wild). Figure 3 shows the number of unigenes up- and down-regulated at each stage. Overall, domesticated TM-1 displayed a much higher level of transcriptional variation between the sampled time points than did the wild yucatanense accession. When all the developmental transitions were included, 12,626 or 5273 genes experienced significant up- or down-regulation in domesticated or wild cotton, respectively (Figure 3). Between 2 and 7 DPA, 8.7% of assayed genes in TM-1 were differentially expressed [3533 unigenes; P-value ≤ 0.05; false discovery rate (FDR) ≤ 0.05], compared to 6.3% (2552 unigenes) in yucatanense. Notably, there was little change in the transcriptome between 7 and 10 DPA in TM-1, a period of active fibre elongation; only two unigenes were differentially expressed in TM-1, whereas 140 unigenes (0.35% of the total) had altered expression in yucatanense. This difference may relate to differences in the fibre elongation curves between 7 and 16 DPA; TM-1 was entering a sustained period of high rate elongation at 7 DPA whereas yucatanense elongation during this period is slower [5]. Far more genes showed altered expression between 10 DPA (during primary wall synthesis) and 20 DPA (when secondary wall thickening was beginning) in both genotypes (Figure 2) [24,25]. During this period, 18.8% (7575) and 6.2% (2516) of the unigenes were differentially expressed in TM-1 and in yucatanense, respectively. As secondary wall deposition continued between 20 to 25 DPA, only 1486 (3.7%) or 45 (0.1%) unigenes changed expression in TM-1 or yucatanense, respectively.

Bottom Line: About 15% of the differentially expressed genes in wild versus domesticated cotton fibre have no homology to the genes in databases.Gene expression during fibre development within accessions and expression alteration arising from evolutionary change appears to be 'modular' - complex genic networks have been simultaneously and similarly transformed, in a coordinated fashion, as a consequence of human-mediated selection.These results highlight the complex alteration of the global gene expression machinery that resulted from human selection for a longer, stronger and finer fibre, as well as other aspects of fibre physiology that were not consciously selected.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology, 251 Bessey Hall, Iowa State University, Ames, IA 50011, USA.

ABSTRACT

Background: Understanding the evolutionary genetics of modern crop phenotypes has a dual relevance to evolutionary biology and crop improvement. Modern upland cotton (Gossypium hirsutum L.) was developed following thousands of years of artificial selection from a wild form, G. hirsutum var. yucatanense, which bears a shorter, sparser, layer of single-celled, ovular trichomes ('fibre'). In order to gain an insight into the nature of the developmental genetic transformations that accompanied domestication and crop improvement, we studied the transcriptomes of cotton fibres from wild and domesticated accessions over a developmental time course.

Results: Fibre cells were harvested between 2 and 25 days post-anthesis and encompassed the primary and secondary wall synthesis stages. Using amplified messenger RNA and a custom microarray platform designed to interrogate expression for 40,430 genes, we determined global patterns of expression during fibre development. The fibre transcriptome of domesticated cotton is far more dynamic than that of wild cotton, with over twice as many genes being differentially expressed during development (12,626 versus 5273). Remarkably, a total of 9465 genes were diagnosed as differentially expressed between wild and domesticated fibres when summed across five key developmental time points. Human selection during the initial domestication and subsequent crop improvement has resulted in a biased upregulation of components of the transcriptional network that are important for agronomically advanced fibre, especially in the early stages of development. About 15% of the differentially expressed genes in wild versus domesticated cotton fibre have no homology to the genes in databases.

Conclusions: We show that artificial selection during crop domestication can radically alter the transcriptional developmental network of even a single-celled structure, affecting nearly a quarter of the genes in the genome. Gene expression during fibre development within accessions and expression alteration arising from evolutionary change appears to be 'modular' - complex genic networks have been simultaneously and similarly transformed, in a coordinated fashion, as a consequence of human-mediated selection. These results highlight the complex alteration of the global gene expression machinery that resulted from human selection for a longer, stronger and finer fibre, as well as other aspects of fibre physiology that were not consciously selected. We illustrate how the data can be mined for genes that were unwittingly targeted by aboriginal and/or modern domesticators during crop improvement and/or which potentially control the improved qualities of domesticated cotton fibre.See Commentary: http://www.biomedcentral.com/1741-7007/8/137.

Show MeSH
Related in: MedlinePlus