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

Males and females of dioecious plants have sex-specific adaptations to diverse habitats. The effects of inter- and intrasexual interactions in poplar plantations on composition, structure, and function of soil microbiota have not been explored in degraded areas. We conducted a series of greenhouse and field experiments to investigate how belowground competition, soil microbial communities, and seasonal variation nitrogen content differ among female, male, and mixed-sex Populus cathayana plantations. In the greenhouse experiment, female neighbors suppressed the growth of males under optimal nitrogen conditions. However, male neighbors enhanced stable isotope ratio of nitrogen (δ15 N) of females under intersexual competition. In the field, the root length density, root area density, and biomass of fine roots were lower in female plantations than in male or mixed-sex plantations. Bacterial networks of female, male, and mixed-sex plantations were characterized by different composition of hub nodes, including connectors, modules, and network hubs. The sex composition of plantations altered bacterial and fungal community structures according to Bray-Curtis distances, with 44% and 65% of variance explained by the root biomass, respectively. The total soil nitrogen content of mixed-sex plantation was higher than that in female plantation in spring and summer. The mixed-sex plantation also had a higher ß-1,4-N-acetyl-glucosaminidase activity in summer and a higher nitrification rate in autumn than the other two plantations. The seasonal soil N content, nitrification rate, and root distribution traits demonstrated spatiotemporal niche separation in the mixed-sex plantation. We argue that a strong female-female competition and limited nitrogen content could strongly impede plant growth and reduce the resistance of monosex plantations to climate change and the mixed-sex plantations constitutes a promising way to restore degraded land.

How does plant sex alter microbiota assembly in dioecious plants?

Plant microbiota can greatly impact plant growth, defense, and health in different environments. Thus, it might be evolutionarily beneficial for plants to be able to control processes related to microbiota assembly. Dioecious plant species display sexual dimorphism in morphology, physiology, and immunity. These differences imply that male and female individuals might differently regulate their microbiota, but the role of sex in microbiota assembly has been largely neglected so far. Here, we introduce the mechanism of how sex controls microbiota in plants analogically to the sex regulation of gut microbiota in animals, in particular in humans. We argue that plant sex imposes selective pressure on filtering and constructing microbiota in the rhizosphere, phyllosphere, and endosphere along the soil-plant continuum. Since male plants are more resistant than female plants to environmental stresses, we suggest that a male host forms more stable and resistant plant microbiota that cooperate more effectively with the host to resist stresses. Male and female plants can distinguish whether a plant is of the same or different sex, and males can alleviate stress-caused damage in females. The impact of a male host on microbiota would protect female plants from unfavorable environments.

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

Selenium (Se) acquirement from daily diet can help reduce the risk of many diseases. The edible parts of crop plants are the main source of dietary Se, while the Se content in crops is determined by Se bioavailability in soil. We summarize recent research on the biogeochemical cycle of Se driven by specific microorganisms and emphasize the oxidizing process in the Se cycle. Moreover, we discuss how plant root exudates and rhizosphere microorganisms affect soil Se availability. Finally, we cover beneficial microorganisms, including endophytes, that promote crop quality and improve crop tolerance to environmental stresses. Se availability to plants depends on the balance between adsorption and desorption, reduction, methylation and oxidation, which are determined by interactions among soil properties, microbial communities and plants. Reduction and methylation processes governed by bacteria or fungi lead to declined Se availability, while Se oxidation regulated by Se-oxidizing microorganisms increases Se availability to plants. Despite a much lower rate of Se oxidization compared to reduction and methylation, the potential roles of microbial communities in increasing Se bioavailability are probably largely underestimated. Enhancing Se oxidation and Se desorption are crucial for the promotion of Se bioavailability and uptake, particularly in Se-deficient soils. Beneficial roles of Se are reported in terms of improved crop growth and quality, and enhanced protection against fungal diseases and abiotic stress through improved photosynthetic traits, increased sugar and amino acid contents, and promoted defense systems. Understanding Se transformation along the plant-soil continuum is crucial for agricultural production and even for human health.

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

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. Video Abstract.

Rhizosphere soil bacterial communities and nitrogen cycling affected by deciduous and evergreen tree species.

Deciduous and evergreen trees differ in their responses to drought and nitrogen (N) demand. Whether or not these functional types affect the role of the bacterial community in the N cycle during drought remains uncertain. Two deciduous tree species (Alnus cremastogyne, an N2-fixing species, and Liquidambar formosana) and two evergreen trees (Cunninghamia lanceolata and Pinus massoniana) were used to assess factors in controlling rhizosphere soil bacterial community and N cycling functions. Photosynthetic rates and biomass production of plants, 16S rRNA sequencing and N-cycling-related genes of rhizosphere soil were measured. The relative abundance of the phyla Actinobacteria and Firmicutes was higher, and that of Proteobacteria, Acidobacteria, and Gemmatimondaetes was lower in rhizosphere soil of deciduous trees than that of evergreen. Beta-diversity of bacterial community also significantly differed between the two types of trees. Deciduous trees showed significantly higher net photosynthetic rates and biomass production than evergreen species both at well water condition and short-term drought. Root biomass was the most important factor in driving soil bacterial community and N-cycling functions than total biomass and aboveground biomass. Furthermore, 44 bacteria genera with a decreasing response and 46 taxa showed an increased response along the root biomass gradient. Regarding N-cycle-related functional genes, copy numbers of ammonia-oxidizing bacteria (AOB) and autotrophic ammonia-oxidizing archaea (AOA), N2 fixation gene (nifH), and denitrification genes (nirK, nirS) were significantly higher in the soil of deciduous trees than in that of the evergreen. Structural equation models explained 50.2%, 47.6%, 48.6%, 49.4%, and 37.3% of the variability in copy numbers of nifH, AOB, AOA, nirK, and nirS, respectively, and revealed that root biomass had significant positive effects on copy numbers of all N-cycle functional genes. In conclusion, root biomass played key roles in affecting bacterial community structure and soil N cycling. Our findings have important implications for our understanding of plants control over bacterial community and N-cycling function in artificial forest ecosystems.

Differences in carbon and nitrogen metabolism between male and female Populus cathayana in response to deficient nitrogen.

Sexual dimorphism occurs regarding carbon and nitrogen metabolic processes in response to nitrogen supply. Differences in fixation and remobilization of carbon and allocation and assimilation of nitrogen between sexes may differ under severe defoliation. The dioecious species Populus cathayana was studied after two defoliation treatments with two N levels. Males had a higher capacity of carbon fixation because of higher gas exchange and fluorescence traits of leaves after severe long-term defoliation under deficient N. Males had higher leaf abscisic acid, stomatal conductance and leaf sucrose phosphate synthase activity increasing transport of sucrose to sinks. Males had a higher carbon sink than females, because under N-deficient conditions, males accumulated >131.10% and 90.65% root starch than males in the control, whereas females accumulated >40.55% and 52.81%, respectively, than females in the control group. Males allocated less non-protein N (NNon-p) to leaves, having higher nitrogen use efficiency (photosynthetic nitrogen use efficiency), higher glutamate dehydrogenase (GDH) and higher leaf GDH expression, even after long-term severe defoliation under deficient N. Females had higher leaf jasmonic acid concentration and NNon-p. The present study suggested that females allocated more carbon and nitrogen to defense chemicals than males after long-term severe defoliation under deficient N.

Rootstock determines the drought resistance of poplar grafting combinations.

To increase yield and/or enhance resistance to diseases, grafting is often applied in agriculture and horticulture. Interspecific grafting could possibly be used in forestry as well to improve drought resistance, but our understanding of how the rootstock of a more drought-resistant species can affect the grafted plant is very limited. Reciprocal grafts of two poplar species, Populus cathayana Rehder (less drought-resistant, C) and Populus deltoides Bart. ex Marsh (more drought-resistant, D) were generated. Four grafting combinations (scion/rootstock: C/C, C/D, D/D and D/C) were subjected to well-watered and drought stress treatments. C/D and D/C had a higher diameter growth rate, leaf biomass, intrinsic water-use efficiency (WUEi) and total non-structural carbohydrate (NSC) content than C/C and D/D in well-watered condition. However, drought caused greater differences between P. deltoides-rooted and P. cathayana-rooted grafting combinations, especially between C/D and D/C. The C/D grafting combination showed higher resistance to drought, as indicated by a higher stem growth rate, net photosynthetic rate, WUEi, leaf water potential, proline concentration and NSC concentration and maintenance of integrity of the leaf cellular ultrastructure under drought when compared with D/C. D/C exhibited severely damaged cell membranes, mitochondria and chloroplasts under drought. The scion genotype caused a strong effect on the root proline concentration: the P. cathayana scion increased the root proline concentration more than the P. deltoides scion (C/C vs D/C and C/D vs D/D) under water deficit. Our results demonstrated that mainly the rootstock was responsible for the drought resistance of grafting combinations. Grafting of the P. cathayana scion onto P. deltoides rootstock resulted in superior growth and biomass when compared with the other three combinations both in well-watered and drought stress conditions.

Physiological and proteomic analysis reveals the different responses of Cunninghamia lanceolata seedlings to nitrogen and phosphorus additions.

UNLABELLED: Both nitrogen (N) and phosphorus (P) additions in soils can increase tree photosynthetic rate (Pn), biomass accumulation and further increase primary production of plantation. However, the improved photosynthetic ability is varied from the added nutrient types and the mechanisms are sophisticated. In this study, an iTRAQ-based quantitative proteome combined with physiological analysis of Chinese fir (Cunninghamia lanceolata) leaves was performed to determine the common and different responses on photosynthetic process to the N and P additions. The results showed that, either N or P added in soils significantly increased Pn, but N addition had more positive effects than P addition in improving photosynthetic ability. Physiologically, N addition caused more in improving photosynthetic rate than P addition, which attributes to higher leaf N and chlorophyll contents, enlarged chloroplast size and more number of thylakoids. Proteomic data revealed that the increased Pn to N and P additions may attribute to the increased abundance of proteins involved in carbon fixation and RuBP regeneration during the light-independent reactions. However, N addition increased the abundance of photosystem II related proteins and P addition increased the abundance of photosystem I related proteins. Additionally, proteomic data also gave some clues on the different metabolic processes caused by N and P additions on glycolysis and TCA cycle, which were potentially related to higher growth and developmental rates of C. lanceolata. Therefore, this study provides new insights into the different photosynthesis and metabolic processes of Chinese fir in response to N and P additions. BIOLOGICAL SIGNIFICANCE: Fertilization is an important management measure to improve timber yield and primary production of Cunninghamia lanceolata, which is the largest planted coniferous species in southeast China. Nitrogen (N) and phosphorus (P) additions into soils can improve tree photosynthesis, and further increase plantation production. However, the mechanism of N and P additions in improving photosynthesis is still unclearly. In this study, a physiological measurement combined with proteomic analysis was performed on a controlled experiment in the greenhouse. These results improve understanding of the essentially photosynthetic activity and metabolic process of C. lanceolata responding to N and P fertilization.