Sex-based metabolic and microbiota differences in roots and rhizosphere soils of dioecious papaya (Carica papaya L.)

Abstract

Dioecious plant species have a high genetic variation that is important for coping with or adapting to environmental stress through natural selection. Intensive studies have reported dimorphism morphism in morphology, physiology, as well as biotic and abiotic stress responses in dioecious plants. Here, we demonstrated the dimorphism of metabolic profile and the preference of some microorganisms in the roots and rhizosphere soils of male and female papaya. The metabolic composition of roots were significantly different between the males and females. Some sex hormones occurred in the differential metabolites in roots and rhizosphere soils. For example, testosterone was up-regulated in male papaya roots and rhizosphere soils, whereas norgestrel was up-regulated in the female papaya roots, indicating a possible balance in papaya roots to control the sexual differentiation. Plant hormones such as BRs, JAs, SA and GAs were also detected among the differential metabolites in the roots and rhizosphere soils of dioecious papaya. In addition, some metabolites that have medicinal values, such as ecliptasaponin A, crocin, berberine and sapindoside A were also expressed differentially between the two sexes. Numerous differential metabolites from the papaya roots were secreted in the soil, resulting in the differences in microbial community structure in the roots and rhizosphere soils. Some nitrogen-fixing bacteria such as Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium, Brevundimonas and Microvirga were enriched in the male papaya roots or rhizosphere soils. While Candidatus Solibacter and Tumebacillus, which utilize organic matters, were enriched in the roots or rhizosphere soils of the female papaya. Some differences in the fungi abundance were also observed in both male and female papaya roots. These findings uncovered the effect of sex types on the metabolic and microbiota differences in roots and rhizosphere soils in papaya and will lead to investigations of underlining genomic and molecular mechanisms.

Identification and Analysis of Antimicrobial Activities from a Model Moss Ceratodon purpureus

“…It would be similarly interesting to analyze the effects of sexual dimorphism in secreted antibacterial compounds on stress response, fitness, or physiological differences in C. purpureus male and female strains. Another implication of our study is that if genetic variation in secreted antibacterial compounds can also be demonstrated for C. purpureus male and female strains in their natural habitats, R40- and GG1-associated microbiomes could also be different, as was recently demonstrated for roots and rhizosphere soils of the dioecious flowering plant Carica papaya [ 36 ].…”

Male, female, and mixed‐sex poplar plantations support divergent soil microbial communities

“…Differences in the physical and chemical traits of the litter or the quality and quantity of root‐deprived compound profiles can lead to divergent microbial communities (Palomino et al., 2023; Zhalnina et al., 2018). Males and females show differences in physical and chemical traits during leaf growth (Guo et al., 2022; Zhang et al., 2014; Zhou et al., 2022), and also different in nutrient resorption efficiency during leaf senescence (Yu, Huang, et al., 2022). The results implied that the leaf litter traits of males and females are different and they may influence microbial communities during the decomposition stage, which would be another interesting topic but not investigated in this study.…”

“…Plants interacting with different neighbors have been shown to induce major changes in soil microbial communities (Guo et al, 2019). Recent studies found that males and females can recruit sex-specific soil microbial communities (Guo et al, 2021(Guo et al, , 2022Vega-Frutis & Guevara, 2009;Zhou et al, 2022;Zhu et al, 2024), which would in turn affect soil nutrient availability and plant growth (Guo et al, 2023). Alterations in belowground interactions between male and female plants or between the same sex plants might further cause important changes in the structure and function of bacterial and fungal communities.…”