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Cassava genome from a wild ancestor to cultivated varieties.

Wang W, Feng B, Xiao J, Xia Z, Zhou X, Li P, Zhang W, Wang Y, Møller BL, Zhang P, Luo MC, Xiao G, Liu J, Yang J, Chen S, Rabinowicz PD, Chen X, Zhang HB, Ceballos H, Lou Q, Zou M, Carvalho LJ, Zeng C, Xia J, Sun S, Fu Y, Wang H, Lu C, Ruan M, Zhou S, Wu Z, Liu H, Kannangara RM, Jørgensen K, Neale RL, Bonde M, Heinz N, Zhu W, Wang S, Zhang Y, Pan K, Wen M, Ma PA, Li Z, Hu M, Liao W, Hu W, Zhang S, Pei J, Guo A, Guo J, Zhang J, Zhang Z, Ye J, Ou W, Ma Y, Liu X, Tallon LJ, Galens K, Ott S, Huang J, Xue J, An F, Yao Q, Lu X, Fregene M, López-Lavalle LA, Wu J, You FM, Chen M, Hu S, Wu G, Zhong S, Ling P, Chen Y, Wang Q, Liu G, Liu B, Li K, Peng M - Nat Commun (2014)

Bottom Line: Our analyses reveal that genes involved in photosynthesis, starch accumulation and abiotic stresses have been positively selected, whereas those involved in cell wall biosynthesis and secondary metabolism, including cyanogenic glucoside formation, have been negatively selected in the cultivated varieties, reflecting the result of natural selection and domestication.Differences in microRNA genes and retrotransposon regulation could partly explain an increased carbon flux towards starch accumulation and reduced cyanogenic glucoside accumulation in domesticated cassava.These results may contribute to genetic improvement of cassava through better understanding of its biology.

View Article: PubMed Central - PubMed

Affiliation: Institute of Tropical Biosciences and Biotechnology, Chinese Academy of Tropical Agricultural Sciences (CATAS), Haikou 571101, China.

ABSTRACT
Cassava is a major tropical food crop in the Euphorbiaceae family that has high carbohydrate production potential and adaptability to diverse environments. Here we present the draft genome sequences of a wild ancestor and a domesticated variety of cassava and comparative analyses with a partial inbred line. We identify 1,584 and 1,678 gene models specific to the wild and domesticated varieties, respectively, and discover high heterozygosity and millions of single-nucleotide variations. Our analyses reveal that genes involved in photosynthesis, starch accumulation and abiotic stresses have been positively selected, whereas those involved in cell wall biosynthesis and secondary metabolism, including cyanogenic glucoside formation, have been negatively selected in the cultivated varieties, reflecting the result of natural selection and domestication. Differences in microRNA genes and retrotransposon regulation could partly explain an increased carbon flux towards starch accumulation and reduced cyanogenic glucoside accumulation in domesticated cassava. These results may contribute to genetic improvement of cassava through better understanding of its biology.

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Cyanogenesis differentiation between wild and cultivated cassava.(a) Minimizing of cyanogenic glucoside content in cultivar KU50 and Arg7 relative to wild W14: over twofold in leaves and fivefold in storage root with five repeat plants. (b) Differential expression of genes in the cyanogenic glucoside synthesis pathway between cultivar KU50, Arg7 and wild W14 identified by RNA-seq. DS, developing stem; ETR, early storage root; LF, leaf; LTR, late storage root; MTR, medium tuber root. (c) A transposon regulation model of cyanogenesis in cassava: among the interval regions of three genes in a linear array as CYP71E11, CYP71E7 and UGT85K4, there were more transposable or retrotransposable elements in the gene 1-kb upstream regions of cultivated species KU50 and AM560 than wild subspecies W14. CDS, Coding sequence.
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f3: Cyanogenesis differentiation between wild and cultivated cassava.(a) Minimizing of cyanogenic glucoside content in cultivar KU50 and Arg7 relative to wild W14: over twofold in leaves and fivefold in storage root with five repeat plants. (b) Differential expression of genes in the cyanogenic glucoside synthesis pathway between cultivar KU50, Arg7 and wild W14 identified by RNA-seq. DS, developing stem; ETR, early storage root; LF, leaf; LTR, late storage root; MTR, medium tuber root. (c) A transposon regulation model of cyanogenesis in cassava: among the interval regions of three genes in a linear array as CYP71E11, CYP71E7 and UGT85K4, there were more transposable or retrotransposable elements in the gene 1-kb upstream regions of cultivated species KU50 and AM560 than wild subspecies W14. CDS, Coding sequence.

Mentions: The latent toxicity caused by cyanogenesis in cassava is clearly a potential health hazard when it is consumed as food. The pathway for cyanogenic glucoside biosynthesis in cassava and the genes encoding the enzymes involved have been elucidated in recent years464748. We determined the linamarin and lotaustralin content in cultivated KU50, Arg7 and wild W14, and found that the linamarin content was reduced six- to tenfold in storage roots and three- to fourfold in leaves of KU50 and Arg7 relative to W14 (Fig. 3a, Supplementary Note 19, Supplementary Table 18). Remarkably, the expression of the genes CYP79D1, CYP79D2, CYP71E7, CYP71E11, UGT85K4 and UGT85K5 that encode the enzymes catalysing linamarin and lotaustralin formation, all exhibited five- to tenfold lower expression levels in the storage roots and leaves of KU50 relative to W14, further suggesting a potential outcome of domestication. Different classes of DNA retrotransposons, like miniature inverted-repeat transposable elements (MITEs) and LTR transposable elements, have been shown to influence the expression of proximal genes, especially if simultaneously situated downstream and upstream of the same gene. In general, gene expression is suppressed by the presence of these elements48. To investigate potential effects of transposons on gene expression in cassava, the 1-kb upstream regions of orthologous genes present in the W14, KU50 and AM560 genomes were analysed for the presence of MITEs. A total of 553 MITEs were found, of which 310 and 243 were uniquely present within the genomes of AM560 and W14, respectively. Among the 310 AM560-specific MITE insertions, 96 (34.5%) showed significantly lower expression and 32 (11.5%) had significantly higher expressions in storage roots or leaves of cultivated varieties when compared with W14 (Supplementary Data 6). We compared the genomic regions containing CYP71E11, CYP71E7 and UGT85K4, and found that these three genes were positioned in a linear array within homologous scaffolds in the three genomes. Two distinct larger insertions containing MITE and LTR transposons were identified to be present in the 5′UTR and 3′UTR regions of those genes in KU50 and AM560, but not in the wild ancestor W14 (Fig. 3c). Taken together, these results suggest that transposon activity may have played a role in the reduction of cyanogenic glucoside content in the domesticated cassava. It remains to be seen how the distribution patterns of transposable elements affect cyanogenic compound biosynthesis in cassava, although transposable elements have been shown to alter the expression patterns of adjacent genes in plant genomes49.


Cassava genome from a wild ancestor to cultivated varieties.

Wang W, Feng B, Xiao J, Xia Z, Zhou X, Li P, Zhang W, Wang Y, Møller BL, Zhang P, Luo MC, Xiao G, Liu J, Yang J, Chen S, Rabinowicz PD, Chen X, Zhang HB, Ceballos H, Lou Q, Zou M, Carvalho LJ, Zeng C, Xia J, Sun S, Fu Y, Wang H, Lu C, Ruan M, Zhou S, Wu Z, Liu H, Kannangara RM, Jørgensen K, Neale RL, Bonde M, Heinz N, Zhu W, Wang S, Zhang Y, Pan K, Wen M, Ma PA, Li Z, Hu M, Liao W, Hu W, Zhang S, Pei J, Guo A, Guo J, Zhang J, Zhang Z, Ye J, Ou W, Ma Y, Liu X, Tallon LJ, Galens K, Ott S, Huang J, Xue J, An F, Yao Q, Lu X, Fregene M, López-Lavalle LA, Wu J, You FM, Chen M, Hu S, Wu G, Zhong S, Ling P, Chen Y, Wang Q, Liu G, Liu B, Li K, Peng M - Nat Commun (2014)

Cyanogenesis differentiation between wild and cultivated cassava.(a) Minimizing of cyanogenic glucoside content in cultivar KU50 and Arg7 relative to wild W14: over twofold in leaves and fivefold in storage root with five repeat plants. (b) Differential expression of genes in the cyanogenic glucoside synthesis pathway between cultivar KU50, Arg7 and wild W14 identified by RNA-seq. DS, developing stem; ETR, early storage root; LF, leaf; LTR, late storage root; MTR, medium tuber root. (c) A transposon regulation model of cyanogenesis in cassava: among the interval regions of three genes in a linear array as CYP71E11, CYP71E7 and UGT85K4, there were more transposable or retrotransposable elements in the gene 1-kb upstream regions of cultivated species KU50 and AM560 than wild subspecies W14. CDS, Coding sequence.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4214410&req=5

f3: Cyanogenesis differentiation between wild and cultivated cassava.(a) Minimizing of cyanogenic glucoside content in cultivar KU50 and Arg7 relative to wild W14: over twofold in leaves and fivefold in storage root with five repeat plants. (b) Differential expression of genes in the cyanogenic glucoside synthesis pathway between cultivar KU50, Arg7 and wild W14 identified by RNA-seq. DS, developing stem; ETR, early storage root; LF, leaf; LTR, late storage root; MTR, medium tuber root. (c) A transposon regulation model of cyanogenesis in cassava: among the interval regions of three genes in a linear array as CYP71E11, CYP71E7 and UGT85K4, there were more transposable or retrotransposable elements in the gene 1-kb upstream regions of cultivated species KU50 and AM560 than wild subspecies W14. CDS, Coding sequence.
Mentions: The latent toxicity caused by cyanogenesis in cassava is clearly a potential health hazard when it is consumed as food. The pathway for cyanogenic glucoside biosynthesis in cassava and the genes encoding the enzymes involved have been elucidated in recent years464748. We determined the linamarin and lotaustralin content in cultivated KU50, Arg7 and wild W14, and found that the linamarin content was reduced six- to tenfold in storage roots and three- to fourfold in leaves of KU50 and Arg7 relative to W14 (Fig. 3a, Supplementary Note 19, Supplementary Table 18). Remarkably, the expression of the genes CYP79D1, CYP79D2, CYP71E7, CYP71E11, UGT85K4 and UGT85K5 that encode the enzymes catalysing linamarin and lotaustralin formation, all exhibited five- to tenfold lower expression levels in the storage roots and leaves of KU50 relative to W14, further suggesting a potential outcome of domestication. Different classes of DNA retrotransposons, like miniature inverted-repeat transposable elements (MITEs) and LTR transposable elements, have been shown to influence the expression of proximal genes, especially if simultaneously situated downstream and upstream of the same gene. In general, gene expression is suppressed by the presence of these elements48. To investigate potential effects of transposons on gene expression in cassava, the 1-kb upstream regions of orthologous genes present in the W14, KU50 and AM560 genomes were analysed for the presence of MITEs. A total of 553 MITEs were found, of which 310 and 243 were uniquely present within the genomes of AM560 and W14, respectively. Among the 310 AM560-specific MITE insertions, 96 (34.5%) showed significantly lower expression and 32 (11.5%) had significantly higher expressions in storage roots or leaves of cultivated varieties when compared with W14 (Supplementary Data 6). We compared the genomic regions containing CYP71E11, CYP71E7 and UGT85K4, and found that these three genes were positioned in a linear array within homologous scaffolds in the three genomes. Two distinct larger insertions containing MITE and LTR transposons were identified to be present in the 5′UTR and 3′UTR regions of those genes in KU50 and AM560, but not in the wild ancestor W14 (Fig. 3c). Taken together, these results suggest that transposon activity may have played a role in the reduction of cyanogenic glucoside content in the domesticated cassava. It remains to be seen how the distribution patterns of transposable elements affect cyanogenic compound biosynthesis in cassava, although transposable elements have been shown to alter the expression patterns of adjacent genes in plant genomes49.

Bottom Line: Our analyses reveal that genes involved in photosynthesis, starch accumulation and abiotic stresses have been positively selected, whereas those involved in cell wall biosynthesis and secondary metabolism, including cyanogenic glucoside formation, have been negatively selected in the cultivated varieties, reflecting the result of natural selection and domestication.Differences in microRNA genes and retrotransposon regulation could partly explain an increased carbon flux towards starch accumulation and reduced cyanogenic glucoside accumulation in domesticated cassava.These results may contribute to genetic improvement of cassava through better understanding of its biology.

View Article: PubMed Central - PubMed

Affiliation: Institute of Tropical Biosciences and Biotechnology, Chinese Academy of Tropical Agricultural Sciences (CATAS), Haikou 571101, China.

ABSTRACT
Cassava is a major tropical food crop in the Euphorbiaceae family that has high carbohydrate production potential and adaptability to diverse environments. Here we present the draft genome sequences of a wild ancestor and a domesticated variety of cassava and comparative analyses with a partial inbred line. We identify 1,584 and 1,678 gene models specific to the wild and domesticated varieties, respectively, and discover high heterozygosity and millions of single-nucleotide variations. Our analyses reveal that genes involved in photosynthesis, starch accumulation and abiotic stresses have been positively selected, whereas those involved in cell wall biosynthesis and secondary metabolism, including cyanogenic glucoside formation, have been negatively selected in the cultivated varieties, reflecting the result of natural selection and domestication. Differences in microRNA genes and retrotransposon regulation could partly explain an increased carbon flux towards starch accumulation and reduced cyanogenic glucoside accumulation in domesticated cassava. These results may contribute to genetic improvement of cassava through better understanding of its biology.

Show MeSH