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The ongoing diversification of plant defence compounds exerts dynamic selection pressures on the microorganisms that colonize plant tissues. Evolutionary processes that generate resistance towards these compounds increase microbial fitness by giving access to plant resources and increasing pathogen virulence. These processes entail sequence-based mechanisms that result in adaptive gene functions, and combinatorial mechanisms that result in novel syntheses of existing gene functions. However, the priority and interactions among these processes in adaptive resistance remain poorly understood. Using a combination of molecular genetic and computational approaches, we investigated the contributions of sequence-based and combinatorial processes to the evolution of fungal metabolic gene clusters encoding stilbene cleavage oxygenases (SCOs), which catalyse the degradation of biphenolic plant defence compounds known as stilbenes into monophenolic molecules. We present phylogenetic evidence of convergent assembly among three distinct types of SCO gene clusters containing alternate combinations of phenolic catabolism. Multiple evolutionary transitions between different cluster types suggest recurrent selection for distinct gene assemblages. By comparison, we found that the substrate specificities of heterologously expressed SCO enzymes encoded in different clusters types were all limited to stilbenes and related molecules with a 4'-OH group, and differed modestly in substrate range and activity under the experimental conditions. Together, this work suggests a primary role for genome structural rearrangement, and the importance of enzyme modularity, in promoting fungal metabolic adaptation to plant defence chemistry.

Cynomorium songaricum Rupr. is a rare root-parasitic plant distributed in the desert ecosystem. Little is known about the role of endophytes in accumulation of metabolites in C. songaricum. Here, the correlations between the seven active components (total sugars, flavonoids, protocatechuic acid, catechins, tannins, gallic acid, and ursolic acid) and the endophytic fungi of C. songaricum were investigated, and their causal relationships are discussed further. The results showed that the accumulation of these components and the assembly of endophytic fungi changed with different plant developmental stages. Diverse relationships including positive and negative correlation were found among chemicals and endophytic fungal operational taxonomic units based on correlation coefficient matrices, which demonstrated that the accumulation of secondary metabolites in C. songaricum is closely related to the endophytic fungal community composition. These results present new opportunities to deeply understand plant-fungal symbioses and secondary metabolite productions.

Regulatory response and interaction of Bradyrhizobium and arbuscular mycorrhizal fungi (AMF) play a vital role in rhizospheric soil processes and productivity of soybean (Glycine max L.). Nitrogen (N) and phosphorus (P) are essential nutrients for plant growth and productivity, the synergistic interaction(s) of AMF and Bradyrhizobium along with rhizospheric beneficial microorganisms stimulate soybean growth and development through enhanced mineral nutrient acquisition (N and P) and improved rhizosphere environment. Such interactions are crucial, especially under low-input eco-friendly agricultural cropping systems, which rely on biological processes rather than agrochemicals to maintain soil quality, sustainability, and productivity. Furthermore, enhancement of N-fixation by root nodules along with AMF-mediated synergism improves plant P nutrition and uptake, and proliferation of phosphate-solubilizing fungi. However, the genetic and/or allelic diversity among native strains, their genes/enzymes and many environmental factors (e.g., soil organic matter, fertilizers, light, temperature, soil moisture, and biotic interactors) affect the interactions between AMF and Bradyrhizobium. New information is available regarding the genetic composition of elite soybean inoculant strains in maximizing symbiotic performance, N-fixing capabilities and depending on N and P status the host-mediated regulation of root architecture. Overall, for sustainable soybean production systems, a deeper understanding of the interaction effects of Bradyrhizobium and AMF co-inoculation are expected in the future, so that optimized combinations of microorganisms can be applied as effective soil inoculants for plant growth promotion and fitness. The objective of this review is to offer insights into the mechanistic interactions of AMF and Bradyrhizobium and rhizopheric soil health, and elucidate the role of environmental factors in regulating growth, development and sustainable soybean productivity.

Cynomorium songaricum Rupr. is a valuable food and medicinal plant with functions, such as an increase in sexual function, mainly attributed to its complex secondary metabolites. However, the effect of internal microbes on metabolite production in C. songaricum is still largely unclear. In this study, the relationship between endophytes and differential secondary metabolites in C. songaricum from seven major producing regions of China were explored based on established methods of metabolomics and high-throughput sequencing. The results showed that there were 13 different marker metabolites, seven shared fungal OTUs, and numerous unshared OTUs among C. songaricum distributed at different locations in China and identified significant correlations between metabolites and endophytic fungi. Our study revealed that endophytic fungi may be one possible factor that can affect the plant secondary metabolite composition.

Significance Arbuscular mycorrhizal (AM) fungi promote phosphorus uptake into host plants in exchange for organic carbon. Physiological tracer experiments showed that up to 100% of acquired phosphate can be delivered to plants via the mycorrhizal phosphate uptake pathway (MPU). Previous studies revealed that the CTTC cis-regulatory element (CRE) is required for promoter activation of mycorrhiza-specific phosphate transporter and H+-ATPase genes. However, the precise transcriptional mechanism directly controlling MPU is unknown. Here, we show that CBX1 binds CTTC and AW-box CREs and coregulates mycorrhizal phosphate transporter and H+-ATPase genes. Interestingly, genes involved in lipid biosynthesis are also regulated by CBX1 through binding to AW box, including RAM2. Our work suggests a common regulatory mechanism underlying complex trait control of symbiotic exchange of nutrients., The arbuscular mycorrhizal (AM) symbiosis, a widespread mutualistic association between land plants and fungi, depends on reciprocal exchange of phosphorus driven by proton-coupled phosphate uptake into host plants and carbon supplied to AM fungi by host-dependent sugar and lipid biosynthesis. The molecular mechanisms and cis-regulatory modules underlying the control of phosphate uptake and de novo fatty acid synthesis in AM symbiosis are poorly understood. Here, we show that the AP2 family transcription factor CTTC MOTIF-BINDING TRANSCRIPTION FACTOR1 (CBX1), a WRINKLED1 (WRI1) homolog, directly binds the evolutionary conserved CTTC motif that is enriched in mycorrhiza-regulated genes and activates Lotus japonicus phosphate transporter 4 (LjPT4) in vivo and in vitro. Moreover, the mycorrhiza-inducible gene encoding H+-ATPase (LjHA1), implicated in energizing nutrient uptake at the symbiotic interface across the periarbuscular membrane, is coregulated with LjPT4 by CBX1. Accordingly, CBX1-defective mutants show reduced mycorrhizal colonization. Furthermore, genome-wide–binding profiles, DNA-binding studies, and heterologous expression reveal additional binding of CBX1 to AW box, the consensus DNA-binding motif for WRI1, that is enriched in promoters of glycolysis and fatty acid biosynthesis genes. We show that CBX1 activates expression of lipid metabolic genes including glycerol-3-phosphate acyltransferase RAM2 implicated in acylglycerol biosynthesis. Our finding defines the role of CBX1 as a regulator of host genes involved in phosphate uptake and lipid synthesis through binding to the CTTC/AW molecular module, and supports a model underlying bidirectional exchange of phosphorus and carbon, a fundamental trait in the mutualistic AM symbiosis.

The demands of feeding a world population are expected to double by 2050. This is because 2.5 billion will be added to the urban population alone. This massive undertaking has posed many challenges toward agricultural productivity and increase in food quality, quantity, and production of protein-rich crops, but on the other hand, modern aggressive agricultural practices have rendered the current acreage of arable land and soil unsustainable to meet the demands of sustainable cropping systems. However, the beneficial role of legumes in cropping systems such as symbiotic nitrogen fixation, intercropping, and rotation of legumes with cereals offers credible potential for providing economically sustainable advantages for farming. The inherent capacity of legumes to form symbiotic associations with biological nitrogen-fixing (BNF) rhizobia and phosphorus-acquiring arbuscular mycorrhizal fungi (AMF), i.e., symbiotic tripartism, further advocates the use of legumes as cover crops, increasing soil fertility, rhizospheric processes, and sustainable (food/oil) crop production. Furthermore, it is estimated that BNF of legumes contribute to five to seven times less greenhouse gas (GHG) emissions per unit area compared to other crops, in addition to estimates of total global BNF of 122 T gN/year (=million tons of N), while AMF play a critical role in global carbon cycle, with estimates of the amount of total C fixed to be up to 20% which is c. 5 T PgC/year (=billion tons of C). In view of this importance of symbiotic tripartism in natural and managed ecosystems, this chapter emphasizes the genetic and symbiotic feature(s) of legumes in large-scale community and global food security programs and soil sustainability and management.