Abstract
BackgroundThe 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.ResultsWe 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.ConclusionsWe 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.
Highlights
The H+-PPase gene family is an important class of proton transporters that play key roles in plant development and stress resistance
Most research on plant H+-PPases has focused on the type I H+-PPases, which are located on the vacuolar membrane and are known as vacuolar proton pyrophosphatases (V-PPase); e.g., Arabidopsis AVP1 (At1g15690) [6,7,8]
All plant species evaluated in the present study contained at least one member of the H+-PPase gene family
Summary
The H+-PPase (pyrophosphatase) gene family is an important class of proton transporters that play key roles in plant development and stress resistance. Overexpression of type I H+-PPase genes can significantly enhance the ability of plants to cope with abiotic stresses, such as anoxia or chilling [11], lack of nutrition [12], drought, and high salt levels [13, 14]. Different members of this gene family may have specific expression in different tissues, organs, or during different developmental stages, but there is currently no compelling evidence to support this [10] Both type I and type II H+PPases have the same active site but have significant differences in subcellular localization and expression levels. Arabidopsis AVP2 (At1g78920, a type II H+PPase) is located in the Golgi apparatus, and its expression level is much lower than that of type I H+-PPases [15]
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