Characterization of Caleosin Genes in Carica papaya and Insights into Lineage-Specific Family Evolution in Brassicales

TL;DR

This study explores the evolution of caleosin genes in papaya and other Brassicales plants, revealing lineage-specific expansions and potential roles in oil accumulation.

Contribution

The first genome-wide analysis of caleosin genes in papaya and insights into their evolutionary expansion in Brassicales.

Findings

Five caleosin genes in papaya represent both H and L clades, with L1 group expansion due to duplication events.

Lineage-specific expansion in Brassicales is linked to tandem duplication, WGDs, and ancient genome triplication.

Tissue-specific expression patterns suggest functional divergence and roles in oil-rich tissues.

Abstract

Caleosins (CLOs) or peroxygenases (PXGs), a class of structural proteins of lipid droplets (LDs), comprise a small family of multifunctional proteins widely involved in oil accumulation, organ development, and stress responses. Despite the proposal of two clades termed H and L in Arabidopsis thaliana, their evolution in the order Brassicales has not been well established. In this study, the first genome-wide analysis of the caleosin family was conducted in papaya (Carica papaya), a Caricaceae plant without any recent whole-genome duplication (WGD). A high number of five members representing both H and L clades were identified from the papaya genome. Further identification and comparison of 68 caleosin genes from 14 representative plant species revealed seven orthogroups, i.e., H1–4 and L1–3, where H1 and L1 have already appeared in the basal angiosperm Amborella trichopoda, supporting their early divergence before angiosperm radiation. Five CpCLO genes belong to H1 (1) and L1 (4), and extensive expansion of the L1 group was shown to be contributed to by species-specific tandem and transposed duplications, which may contribute to environmental adaptation. Orthologous and syntenic analyses uncovered that lineage-specific expansion of the caleosin family in Brassicales relative to A. trichopoda was largely contributed to by tandem duplication and recent WGDs, as well as the ancient γ whole-genome triplication (WGT) shared by all core eudicots. Independent gain or loss of certain introns and apparent expression divergence of caleosin genes were also observed. Tissue-specific expression analysis showed that CpCLO2 and −5 are constitutively expressed, whereas others appear to be tissue-specific, implying function divergence. Interestingly, the H-forms CpCLO1 and RcCLO1 were shown to exhibit similar expression profiles to most oleosin genes that are preferentially expressed oil-rich tissues such as seeds/endosperms, shoots, and calluses, implying their putative involvement in oil accumulation, as observed in Arabidopsis. The results obtained from this study provide a global view of CpCLO genes and insights into lineage-specific family evolution in Brassicales, which facilitates further functional studies in papaya and other non-model species.

Figures