Dataset Information

Lineage-Specific Evolutionary Histories and Regulation of Major Starch Metabolism Genes during Banana Ripening.

ABSTRACT: Starch is the most widespread and abundant storage carbohydrate in plants. It is also a major feature of cultivated bananas as it accumulates to large amounts during banana fruit development before almost complete conversion to soluble sugars during ripening. Little is known about the structure of major gene families involved in banana starch metabolism and their evolution compared to other species. To identify genes involved in banana starch metabolism and investigate their evolutionary history, we analyzed six gene families playing a crucial role in plant starch biosynthesis and degradation: the ADP-glucose pyrophosphorylases (AGPases), starch synthases (SS), starch branching enzymes (SBE), debranching enzymes (DBE), ?-amylases (AMY) and ?-amylases (BAM). Using comparative genomics and phylogenetic approaches, these genes were classified into families and sub-families and orthology relationships with functional genes in Eudicots and in grasses were identified. In addition to known ancestral duplications shaping starch metabolism gene families, independent evolution in banana and grasses also occurred through lineage-specific whole genome duplications for specific sub-families of AGPase, SS, SBE, and BAM genes; and through gene-scale duplications for AMY genes. In particular, banana lineage duplications yielded a set of AGPase, SBE and BAM genes that were highly or specifically expressed in banana fruits. Gene expression analysis highlighted a complex transcriptional reprogramming of starch metabolism genes during ripening of banana fruits. A differential regulation of expression between banana gene duplicates was identified for SBE and BAM genes, suggesting that part of starch metabolism regulation in the fruit evolved in the banana lineage.

SUBMITTER: Jourda C

PROVIDER: S-EPMC5133247 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Lineage-Specific Evolutionary Histories and Regulation of Major Starch Metabolism Genes during Banana Ripening.

Jourda Cyril C Cardi Céline C Gibert Olivier O Giraldo Toro Andrès A Ricci Julien J Mbéguié-A-Mbéguié Didier D Yahiaoui Nabila N

Frontiers in plant science 20161202

Starch is the most widespread and abundant storage carbohydrate in plants. It is also a major feature of cultivated bananas as it accumulates to large amounts during banana fruit development before almost complete conversion to soluble sugars during ripening. Little is known about the structure of major gene families involved in banana starch metabolism and their evolution compared to other species. To identify genes involved in banana starch metabolism and investigate their evolutionary history ...[more]

PMID: 27994606

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Project description:Six MaMADS-box genes have been cloned from the banana fruit cultivar Grand Nain. The similarity of these genes to tomato LeRIN is low and neither MaMADS2 nor MaMADS1 complement the tomato rin mutation. Nevertheless, the expression patterns, specifically in fruit and the induction during ripening and in response to ethylene and 1-MCP, suggest that some of these genes may participate in ripening. MaMADS1, 2, and 3, are highly expressed in fruit only, while the others are expressed in fruit as well as in other organs. Moreover, the suites of MaMADS-box genes and their temporal expression differ in peel and pulp during ripening. In the pulp, the increase in MaMADS2, 3, 4, and 5 expression preceded an increase in ethylene production, but coincides with the CO(2) peak. However, MaMADS1 expression in pulp coincided with ethylene production, but a massive increase in its expression occurred late during ripening, together with a second wave in the expression of MaMADS2, 3, and 4. In the peel, on the other hand, an increase in expression of MaMADS1, 3, and to a lesser degree also of MaMADS4 and 2 coincided with an increase in ethylene production. Except MaMADS3, which was induced by ethylene in pulp and peel, only MaMADS4, and 5 in pulp and MaMADS1 in peel were induced by ethylene. 1-MCP applied at the onset of the increase in ethylene production, increased the levels of MaMADS4 and MaMADS1 in pulp, while it decreased MaMADS1, 3, 4, and 5 in peel, suggesting that MaMADS4 and MaMADS1 are negatively controlled by ethylene at the onset of ethylene production only in pulp. Only MaMADS2 is neither induced by ethylene nor by 1-MCP, and it is expressed mainly in pulp. Our results suggest that two independent ripening programs are employed in pulp and peel which involve the activation of mainly MaMADS2, 4, and 5 and later on also MaMADS1 in pulp, and mainly MaMADS1, and 3 in peel. Hence, our results are consistent with MaMADS2, a SEP3 homologue, acting in the pulp upstream of the increase in ethylene production similarly to LeMADS-RIN.

Project description:BACKGROUND: Banana is one of the most important crop plants grown in the tropics and sub-tropics. It is a climacteric fruit and undergoes ethylene dependent ripening. Once ripening is initiated, it proceeds at a fast rate making postharvest life short, which can result in heavy economic losses. During the fruit ripening process a number of physiological and biochemical changes take place and thousands of genes from various metabolic pathways are recruited to produce a ripe and edible fruit. To better understand the underlying mechanism of ripening, we undertook a study to evaluate global changes in the transcriptome of the fruit during the ripening process. RESULTS: We sequenced the transcriptomes of the unripe and ripe stages of banana (Musa accuminata; Dwarf Cavendish) fruit. The transcriptomes were sequenced using a 454 GSFLX-Titanium platform that resulted in more than 7,00,000 high quality (HQ) reads. The assembly of the reads resulted in 19,410 contigs and 92,823 singletons. A large number of the differentially expressed genes identified were linked to ripening dependent processes including ethylene biosynthesis, perception and signalling, cell wall degradation and production of aromatic volatiles. In the banana fruit transcriptomes, we found transcripts included in 120 pathways described in the KEGG database for rice. The members of the expansin and xyloglucan transglycosylase/hydrolase (XTH) gene families were highly up-regulated during ripening, which suggests that they might play important roles in the softening of the fruit. Several genes involved in the synthesis of aromatic volatiles and members of transcription factor families previously reported to be involved in ripening were also identified. CONCLUSIONS: A large number of differentially regulated genes were identified during banana fruit ripening. Many of these are associated with cell wall degradation and synthesis of aromatic volatiles. A large number of differentially expressed genes did not align with any of the databases and might be novel genes in banana. These genes can be good candidates for future studies to establish their role in banana fruit ripening. The datasets developed in this study will help in developing strategies to manipulate banana fruit ripening and reduce post harvest losses.

Dataset Information

Lineage-Specific Evolutionary Histories and Regulation of Major Starch Metabolism Genes during Banana Ripening.

Publications

Lineage-Specific Evolutionary Histories and Regulation of Major Starch Metabolism Genes during Banana Ripening.

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