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The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants.

ABSTRACT: BACKGROUND:The H+-PPase (pyrophosphatase) gene family is an important class of proton transporters that play key roles in plant development and stress resistance. Although the physiological and biochemical functions of H+-PPases are well characterized, the structural evolution and functional differentiation of this gene family remain unclear. RESULTS:We identified 124 H+-PPase members from 27 plant species using complete genomic data obtained from algae to angiosperms. We found that all analyzed plants carried H+-PPase genes, and members were not limited to the two main types (type I and II). Differentiation of this gene family occurred early in evolutionary history, probably prior to the emergence of algae. The type I and II H+-PPase genes were retained during the subsequent evolution of higher plants, and their copy numbers increased rapidly in some angiosperms following whole-genome duplication (WGD) events, with obvious expression pattern differentiation among the new copies. We found significant functional divergence between type I and II H+-PPase genes, with both showing evidence for positive selection pressure. We classified angiosperm type I H+-PPases into subtypes Ia and non-Ia, which probably differentiated at an early stage of angiosperm evolution. Compared with non-Ia subtype, the Ia subtype appears to confer some advantage in angiosperms, as it is highly conserved and abundantly expressed, but shows no evidence for positive selection. CONCLUSIONS:We hypothesized that there were many types of H+-PPase genes in the plant ancestral genome, and that different plant groups retained different types of these genes. In the early stages of angiosperm evolution, the type I H+-PPase genes differentiated into various subtypes. In addition, the expression pattern varied not only among genes of different types or subtypes, but also among copies of the same subtype. Based on the expression patterns and copy numbers of H+-PPase genes in higher plants, we propose two possible evolutionary trajectories for this gene family.

SUBMITTER: Zhang Y

PROVIDER: S-EPMC7053079 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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The structure, functional evolution, and evolutionary trajectories of the H<sup>+</sup>-PPase gene family in plants.

Zhang Yiming Y Feng Xue X Wang Lihui L Su Yanping Y Chu Zhuodong Z Sun Yanxiang Y

BMC genomics 20200302 1

<h4>Background</h4>The H<sup>+</sup>-PPase (pyrophosphatase) gene family is an important class of proton transporters that play key roles in plant development and stress resistance. Although the physiological and biochemical functions of H<sup>+</sup>-PPases are well characterized, the structural evolution and functional differentiation of this gene family remain unclear.<h4>Results</h4>We identified 124 H<sup>+</sup>-PPase members from 27 plant species using complete genomic data obtained from ...[more]

PMID: 32122295

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Project description:BackgroundThe 12-oxo-phytodienoic acid reductases (OPRs) are enzymes that catalyze the reduction of double-bonds in alpha, beta-unsaturated aldehydes or ketones and are part of the octadecanoid pathway that converts linolenic acid to jasmonic acid. In plants, OPRs belong to the old yellow enzyme family and form multigene families. Although discoveries about this family in Arabidopsis and other species have been reported in some studies, the evolution and function of multiple OPRs in plants are not clearly understood.ResultsA comparative genomic analysis was performed to investigate the phylogenetic relationship, structural evolution and functional divergence among OPR paralogues in plants. In total, 74 OPR genes were identified from 11 species representing the 6 major green plant lineages: green algae, mosses, lycophytes, gymnosperms, monocots and dicots. Phylogenetic analysis showed that seven well-conserved subfamilies exist in plants. All OPR genes from green algae were clustered into a single subfamily, while those from land plants fell into six other subfamilies, suggesting that the events leading to the expansion of the OPR family occurred in land plants. Further analysis revealed that lineage-specific expansion, especially by tandem duplication, contributed to the current OPR subfamilies in land plants after divergence from aquatic plants. Interestingly, exon/intron structure analysis showed that the gene structures of OPR paralogues exhibits diversity in intron number and length, while the intron positions and phase were highly conserved across different lineage species. These observations together with the phylogenetic tree revealed that successive single intron loss, as well as indels within introns, occurred during the process of structural evolution of OPR paralogues. Functional divergence analysis revealed that altered functional constraints have occurred at specific amino acid positions after diversification of the paralogues. Most notably, significant functional divergence was also found in all pairs, except for the II/IV, II/V and V/VI pairs. Strikingly, analysis of the site-specific profiles established by posterior probability revealed that the positive-selection sites and/or critical amino acid residues for functional divergence are mainly distributed in alpha-helices and substrate binding loop (SBL), indicating the functional importance of these regions for this protein family.ConclusionThis study highlights the molecular evolution of the OPR gene family in all plant lineages and indicates critical amino acid residues likely relevant for the distinct functional properties of the paralogues. Further experimental verification of these findings may provide valuable information on the OPRs' biochemical and physiological functions.

Dataset Information

The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants.

Publications

The structure, functional evolution, and evolutionary trajectories of the H<sup>+</sup>-PPase gene family in plants.

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