Dataset Information

Inter-genomic DNA Exchanges and Homeologous Gene Silencing Shaped the Nascent Allopolyploid Coffee Genome (Coffea arabica L.).

ABSTRACT: Allopolyploidization is a biological process that has played a major role in plant speciation and evolution. Genomic changes are common consequences of polyploidization, but their dynamics over time are still poorly understood. Coffea arabica, a recently formed allotetraploid, was chosen to study genetic changes that accompany allopolyploid formation. Both RNA-seq and DNA-seq data were generated from two genetically distant C. arabica accessions. Genomic structural variation was investigated using C. canephora, one of its diploid progenitors, as reference genome. The fate of 9047 duplicate homeologous genes was inferred and compared between the accessions. The pattern of SNP density along the reference genome was consistent with the allopolyploid structure. Large genomic duplications or deletions were not detected. Two homeologous copies were retained and expressed in 96% of the genes analyzed. Nevertheless, duplicated genes were found to be affected by various genomic changes leading to homeolog loss or silencing. Genetic and epigenetic changes were evidenced that could have played a major role in the stabilization of the unique ancestral allotetraploid and its subsequent diversification. While the early evolution of C. arabica mainly involved homeologous crossover exchanges, the later stage appears to have relied on more gradual evolution involving gene conversion and homeolog silencing.

SUBMITTER: Lashermes P

PROVIDER: S-EPMC5015950 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Inter-genomic DNA Exchanges and Homeologous Gene Silencing Shaped the Nascent Allopolyploid Coffee Genome (Coffea arabica L.).

Lashermes Philippe P Hueber Yann Y Combes Marie-Christine MC Severac Dany D Dereeper Alexis A

G3 (Bethesda, Md.) 20160908 9

Allopolyploidization is a biological process that has played a major role in plant speciation and evolution. Genomic changes are common consequences of polyploidization, but their dynamics over time are still poorly understood. Coffea arabica, a recently formed allotetraploid, was chosen to study genetic changes that accompany allopolyploid formation. Both RNA-seq and DNA-seq data were generated from two genetically distant C. arabica accessions. Genomic structural variation was investigated usi ...[more]

PMID: 27440920

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Project description:Background: Polyploidy has long been recognized as an important mechanism in eukaryotes evolution. Recent studies have documented dynamic changes in plant polyploid gene expression, which reflects genomic and functional plasticity of duplicate genes and genomes in plants. Genomewide approaches in a variety of allopolyploids, mostly synthetics, reveal a trend of non-additive gene expression. The aim of the study was to document expression divergence between a relatively recently formed natural allopolyploid (Coffea arabica) and its ancestral parents (Coffea canephora and Coffea eugenioides) and to verify if the divergence was ‘environment-dependent’.Results: Employing a microarray platform designed against 15,522 unigenes, we assayed gene expression levels in allopolyploid and its two parental diploids. For each gene, we determined expression variation levels between the three species grown under two sets of temperature conditions (26-22°C/30-26°C). More than 35% of genes were differentially expressed in each comparison at both temperatures, except for ‘allopolyploid versus Canephora’ at the ‘hottest’ temperature where an unexpected low gene expression divergence (<9%) were observed. Genes were binned in categories: ‘no change’, ‘additivity’, ‘transgressive’ and ‘dominance’ (‘Canephora-like’ and ‘Eugenioides-like’). The totally new phenomenon revealed by our study was a drastic modification of proportions between the allopolyploid and its parents when environmental conditions were modified. At the ‘hottest’ temperature, we found a virtual disappearance of gene categories classed as ‘transgressive’, ‘Eugenioides-like dominance’ or ‘additivity’ and a major increase in genes classed in the ‘Canephora-like dominance’ category. At this set of growing conditions, we therefore found very high bias that suggested a phenomenon of ‘dominance’ of C. canephora transcription profile. The Canephora genome parental expression state seems exhibited in strong preference to the Eugenioides genome parental state. Conclusion: Our data constitute evidence for a transcription profile divergence between allopolyploid and its parental species, massively affected by environmental conditions. The parental origin of the transcription profiles was not consistently biased towards one parental species, but appeared to be affected by environmental conditions. This phenomenon indicates the plasticity of allopolyploids and might ultimately explain better adaptation to environmental conditions.

Project description:BACKGROUND: In higher plants, the inhibition of photosynthetic capacity under drought is attributable to stomatal and non-stomatal (i.e., photochemical and biochemical) effects. In particular, a disruption of photosynthetic metabolism and Rubisco regulation can be observed. Several studies reported reduced expression of the RBCS genes, which encode the Rubisco small subunit, under water stress. RESULTS: Expression of the RBCS1 gene was analysed in the allopolyploid context of C. arabica, which originates from a natural cross between the C. canephora and C. eugenioides species. Our study revealed the existence of two homeologous RBCS1 genes in C. arabica: one carried by the C. canephora sub-genome (called CaCc) and the other carried by the C. eugenioides sub-genome (called CaCe). Using specific primer pairs for each homeolog, expression studies revealed that CaCe was expressed in C. eugenioides and C. arabica but was undetectable in C. canephora. On the other hand, CaCc was expressed in C. canephora but almost completely silenced in non-introgressed ("pure") genotypes of C. arabica. However, enhanced CaCc expression was observed in most C. arabica cultivars with introgressed C. canephora genome. In addition, total RBCS1 expression was higher for C. arabica cultivars that had recently introgressed C. canephora genome than for "pure" cultivars. For both species, water stress led to an important decrease in the abundance of RBCS1 transcripts. This was observed for plants grown in either greenhouse or field conditions under severe or moderate drought. However, this reduction of RBCS1 gene expression was not accompanied by a decrease in the corresponding protein in the leaves of C. canephora subjected to water withdrawal. In that case, the amount of RBCS1 was even higher under drought than under unstressed (irrigated) conditions, which suggests great stability of RBCS1 under adverse water conditions. On the other hand, for C. arabica, high nocturnal expression of RBCS1 could also explain the accumulation of the RBCS1 protein under water stress. Altogether, the results presented here suggest that the content of RBCS was not responsible for the loss of photosynthetic capacity that is commonly observed in water-stressed coffee plants. CONCLUSION: We showed that the CaCe homeolog was expressed in C. eugenioides and non-introgressed ("pure") genotypes of C. arabica but that it was undetectable in C. canephora. On the other hand, the CaCc homeolog was expressed in C. canephora but highly repressed in C. arabica. Expression of the CaCc homeolog was enhanced in C. arabica cultivars that experienced recent introgression with C. canephora. For both C. canephora and C. arabica species, total RBCS1 gene expression was highly reduced with WS. Unexpectedly, the accumulation of RBCS1 protein was observed in the leaves of C. canephora under WS, possibly coming from nocturnal RBCS1 expression. These results suggest that the increase in the amount of RBCS1 protein could contribute to the antioxidative function of photorespiration in water-stressed coffee plants.

Dataset Information

Inter-genomic DNA Exchanges and Homeologous Gene Silencing Shaped the Nascent Allopolyploid Coffee Genome (Coffea arabica L.).

Publications

Inter-genomic DNA Exchanges and Homeologous Gene Silencing Shaped the Nascent Allopolyploid Coffee Genome (Coffea arabica L.).

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