Analysis of Carica papaya Informs Lineage-Specific Evolution of the Aquaporin (AQP) Family in Brassicales

Abstract

Aquaporins (AQPs), a type of intrinsic membrane proteins that transport water and small solutes across biological membranes, play crucial roles in plant growth and development. This study presents a first genome-wide identification and comparative analysis of the AQP gene family in papaya (Carica papaya L.), an economically and nutritionally important fruit tree of tropical and subtropical regions. A total of 29 CpAQP genes were identified, which represent five subfamilies, i.e., nine plasma intrinsic membrane proteins (PIPs), eight tonoplast intrinsic proteins (TIPs), seven NOD26-like intrinsic proteins (NIPs), two X intrinsic proteins (XIPs), and three small basic intrinsic proteins (SIPs). Although the family is smaller than the 35 members reported in Arabidopsis, it is highly diverse, and the presence of CpXIP genes as well as orthologs in Moringa oleifera and Bretschneidera sinensis implies that the complete loss of the XIP subfamily in Arabidopsis is lineage-specific, sometime after its split with papaya but before Brassicaceae–Cleomaceae divergence. Reciprocal best hit-based sequence comparison of 530 AQPs and synteny analyses revealed that CpAQP genes belong to 29 out of 61 identified orthogroups, and lineage-specific evolution was frequently observed in Brassicales. Significantly, the well-characterized NIP3 group was completely lost; lineage-specific loss of the NIP8 group in Brassicaceae occurred sometime before the divergence with Cleomaceae, and lineage-specific loss of NIP2 and SIP3 groups in Brassicaceae occurred sometime after the split with Cleomaceae. In contrast to a predominant role of recent whole-genome duplications (WGDs) on the family expansion in B. sinensis, Tarenaya hassleriana, and Brassicaceae plants, no recent AQP repeats were identified in papaya, and ancient WGD repeats are mainly confined to the PIP subfamily. Subfamily even group-specific evolution was uncovered via comparing exon–intron structures, conserved motifs, the aromatic/arginine selectivity filter, and gene expression profiles. Moreover, down-regulation during fruit ripening and expression divergence of duplicated CpAQP genes were frequently observed in papaya. These findings will not only improve our knowledge on lineage-specific family evolution in Brassicales, but also provide valuable information for further studies of AQP genes in papaya and species beyond.

TIP aquaporins in Cyperus esculentus: genome-wide identification, expression profiles, subcellular localizations, and interaction patterns

“…The ρ WGD identified in rice is Poaceae-specific, whereas τ and σ WGDs are shared by Cyperaceae plants, which may also experience at least one recent WGD [ 22 , 23 , 44 – 46 ]. Wide presence of five phylogenetic groups in both monocots and eudicots [ 3 , 4 , 16 , 36 , 40 , 47 – 49 , Additional file 3 ] support their early diversification. Interestingly, our data from synteny analyses provides the first evidence that both TIP4 and − 5 were derived from TIP2 via WGDs, occurred sometime before monocot-eudicot divergence.…”

Integrative Analysis of Oleosin Genes Provides Insights into Lineage-Specific Family Evolution in Brassicales

“…Genomic sequences of A. trichopoda (v2.1; Amborellaceae, Amborellales), avocado (Gwen v1; Lauraceae, Laurales), A. coerulea (v3.1; Ranunculaceae, Ranunculales), papaya (Sunset v1; Caricaceae, Brassicales), B. sinensis (v1; Akaniaceae, Brassicales), horseradish (v1; Moringaceae, Brassicales), caperbush (v1; Capparaceae, Brassicales), C. violacea (v2.1; Cleomaceae, Brassicales), acaya (v1; Cleomaceae, Brassicales), and spider flower (v1; Cleomaceae, Brassicales) were downloaded from public databases, i.e., Phytozome (v13, , accessed on 31 October 2023), NGDC ( , accessed on 31 October 2023), and NCBI ( , accessed on 31 October 2023). To identify oleosin homologs, the oleosin domain profile (PF01277) was used for HMMER (v3.3, , accessed on 31 October 2023) searches as described before [ 45 , 46 ]. All predicted gene models were manually curated with available mRNAs, including nucleotides, Sanger-expressed sequence tags (ESTs), and RNA sequencing (RNA-seq) reads that were accessed from NCBI (accessed on 31 November 2023).…”

“…html, accessed on 31 October 2023), NGDC (http://bigd.big.ac.cn/gsa, accessed on 31 October 2023), and NCBI (https://www.ncbi.nlm.nih.gov/, accessed on 31 October 2023). To identify oleosin homologs, the oleosin domain profile (PF01277) was used for HMMER (v3.3, http://hmmer.janelia.org/, accessed on 31 October 2023) searches as described before [45,46]. All predicted gene models were manually curated with available mRNAs, including nucleotides, Sanger-expressed sequence tags (ESTs), and RNA sequencing (RNAseq) reads that were accessed from NCBI (accessed on 31 November 2023).…”