Genome-Wide Identification of the Plasma Membrane H+-ATPase in Poplar and Their Responses to Abiotic Stresses and Nitrogen Availability

Plasma membrane (PM) H+-ATPase (HA) plays critical roles in plant growth, development, and stress responses, whereas few studies have focused on the HA gene family in poplar. In this study, 13 HA genes were identified from each of the two haplotype genomes of 717 poplar (Populus tremula × P. alba 717-1B4), and all identified HA proteins in 717 poplar contained three conserved functional domains. Cis-element analysis revealed that promoters of 717 poplar HA genes contained a large number of light-, stress-, and hormone-responsive cis-elements. Transcriptome data showed that P. trichocarpa PtrHA5 and PtrHA7 specifically responded to short-term heat and long-term drought stress in stems and roots, respectively, while PtrHA3 and PtrHA10 responded to multiple abiotic stresses in roots, stems, and leaves. In 717 poplar, PtaHA9 was significantly down-regulated in roots under low-nitrate conditions and up-regulated under high-nitrate conditions. Co-expression network analysis in P. trichocarpa indicated that PtrHA9 had the largest number of co-expressed genes and shared overlapping co-expressed genes with other PtrHA genes. GO and KEGG enrichment analyses of genes within the co-expression network suggested that genes co-expressed with PtrHAs were enriched in energy metabolism, enzyme-activity regulation, and transmembrane substance transport. Collectively, this study systematically characterized the evolutionary and expression profiles of the HA gene family in 717 poplar and suggests putative functional associations of HA genes with poplar stress adaptation.