Plant sex affects plant-microbiome assemblies of dioecious Populus cathayana trees under different soil nitrogen conditions

Abstract

Background Dioecious plants have coevolved with diverse plant microbiomes, which are crucial for the fitness and productivity of their host. Sexual dimorphism in morphology, physiology, or gene expression may relate to different microbial compositions that affect male and female fitness in different environments. However, sex-specific impacts on ecological processes that control the microbiome assembly are not well known. In this study, Populus cathayana males and females were planted in different nitrogen conditions. It was hypothesized that males and females differently affect bacterial and fungal communities in the rhizosphere soil, roots, old leaves, and young leaves. Physiological traits and transcriptome profiles of male and female plants were investigated to reveal potential mechanisms that control the microbiome assembly. Results Our results showed strong niche differentiation that shapes microbial communities leading to a rapid loss of diversity along a decreasing pH gradient from the rhizosphere soil to leaves. Sex had different impacts on the microbial assembly in each niche. Especially fungal endophytes showed great differences in the community structure, keystone species, and community complexity between P. cathayana males and females. For example, the fungal co-occurrence network was more complex and the alpha diversity was significantly higher in young female leaves compared to young male leaves. Transcriptome profiles revealed substantial differences in plant-pathogen interactions and physiological traits that clearly demonstrated divergent internal environments for endophytes inhabiting males and females. Starch and pH of young leaves significantly affected the abundance of Proteobacteria, while tannin and pH of roots showed significant effects on the abundance of Chloroflexi, Actinobacteria, and Proteobacteria, and on the bacterial Shannon diversity. Conclusion Our results provided important knowledge for understanding sexual dimorphism that affects microbial assemblies, thus advancing our understanding of plant-microbiome interactions.

Rapid biodegradation of atrazine by a novel Paenarthrobacter ureafaciens ZY and its effects on soil native microbial community dynamic

“…OTUs belonging to Sphingomonas in P. ureafaciens ZY inoculation treatments, and OTUs belonging to Gaiellales and Sericytochromatia in atrazine alone treatments were more connected with others ( Supplementary Figure S7 ). Guo et al (2022) found that hub species in microbial networks are recognized as mediators among associated microbiome. Trough network hubs, it follows that P. ureafaciens ZY inoculation may influence the assembly of soil native microbial community by regulating microbe-microbe interactions ( Trivedi et al, 2020 ).…”

Selenium species transforming along soil–plant continuum and their beneficial roles for horticultural crops

“…Endophytic selenobacteria, such as Alcaligenes faecalis and S. maltophilia , and especially Paraburkholderia megapolitana , greatly improve the growth of Glycine max under drought because of exogenous Se application [ 126 ]. The endophytes successfully colonize plant roots and leaves probably through overcoming or escaping the plants’ immune system [ 129 ]. Some studies suggest that the metabolism and immune-related traits of plants are key factors in regulating or selecting a specific microbiota that contribute to stress resistance [ 129 , 130 ].…”

“…The endophytes successfully colonize plant roots and leaves probably through overcoming or escaping the plants’ immune system [ 129 ]. Some studies suggest that the metabolism and immune-related traits of plants are key factors in regulating or selecting a specific microbiota that contribute to stress resistance [ 129 , 130 ]. The Se application largely influences plants’ physiological and transcriptome traits [ 131 , 132 ], and probably imposes selective pressure to form specific endophytic communities related with stress resistance.…”

Drought stress‐mediated differences in phyllosphere microbiome and associated pathogen resistance between male and female poplars

“…However, the phyllosphere‐associated microbiome is affected by several abiotic factors such as water availability, soil nutrient limitation, or heavy metal stress as the phyllosphere is an open environment (Gomes et al., 2018; Guo et al., 2022; Liu et al., 2021). As a result of human activities and environmental deterioration, global ecosystems are undergoing rapid climate change that further influences the interactions among plants, microorganisms, and the environment (Zhu et al., 2022).…”