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 functiona...
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doaj-3b557b46d13b49eb975de01ccd0435e92020-11-25T02:25:13ZengBMCBMC Genomics1471-21642020-03-0121111710.1186/s12864-020-6604-2The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plantsYiming Zhang0Xue Feng1Lihui Wang2Yanping Su3Zhuodong Chu4Yanxiang Sun5College of Life Sciences, Langfang Normal UniversityCollege of Life Sciences, Langfang Normal UniversityCollege of Plant Protection, Fujian Agricultural and Forestry UniversityCollege of Life Sciences, Langfang Normal UniversityCollege of Life Sciences, Langfang Normal UniversityCollege of Life Sciences, Langfang Normal UniversityAbstract 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.http://link.springer.com/article/10.1186/s12864-020-6604-2H+-PPase gene familyDuplication eventsFunctional divergencePositive selectionEvolutionary trajectories |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Yiming Zhang Xue Feng Lihui Wang Yanping Su Zhuodong Chu Yanxiang Sun |
spellingShingle |
Yiming Zhang Xue Feng Lihui Wang Yanping Su Zhuodong Chu Yanxiang Sun The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants BMC Genomics H+-PPase gene family Duplication events Functional divergence Positive selection Evolutionary trajectories |
author_facet |
Yiming Zhang Xue Feng Lihui Wang Yanping Su Zhuodong Chu Yanxiang Sun |
author_sort |
Yiming Zhang |
title |
The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants |
title_short |
The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants |
title_full |
The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants |
title_fullStr |
The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants |
title_full_unstemmed |
The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants |
title_sort |
structure, functional evolution, and evolutionary trajectories of the h+-ppase gene family in plants |
publisher |
BMC |
series |
BMC Genomics |
issn |
1471-2164 |
publishDate |
2020-03-01 |
description |
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. |
topic |
H+-PPase gene family Duplication events Functional divergence Positive selection Evolutionary trajectories |
url |
http://link.springer.com/article/10.1186/s12864-020-6604-2 |
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