Loss of the accessory chromosome converts a pathogenic tree-root fungus into a mutualistic endophyte.

Some fungal accessory chromosomes (ACs) may contribute to virulence in plants. However, the mechanisms by which ACs determine specific traits associated with lifestyle transitions along a symbiotic continuum are not clear. Here we delineated the genetic divergence in two sympatric but considerably variable isolates (16B and 16W) of the poplar-associated fungus Stagonosporopsis rhizophilae. We identified a âˆ¼0.6-Mb horizontally acquired AC in 16W that resulted in a mildly parasitic lifestyle in plants. Complete deletion of the AC (Δ16W) significantly altered the fungal phenotype. Specifically, Δ16W was morphologically more similar to 16B, showed enhanced melanization, and established beneficial interactions with poplar plants, thereby acting as a dark septate endophyte. RNA sequencing (RNA-seq) analysis showed that AC loss induced the upregulation of genes related to root colonization and biosynthesis of indole acetic acid and melanin. We observed that the AC maintained a more open status of chromatin across the genome, indicating an impressive remodeling of cis-regulatory elements upon AC loss, which potentially enhanced symbiotic effectiveness. We demonstrated that the symbiotic capacities were non-host-specific through comparable experiments on Triticum- and Arabidopsis-fungus associations. Furthermore, the three isolates generated symbiotic interactions with a nonvascular liverwort. In summary, our study suggests that the AC is a suppressor of symbiosis and provides insights into the underlying mechanisms of mutualism with vascular plants in the absence of traits encoded by the AC. We speculate that AC-situated effectors and other potential secreted molecules may have evolved to specifically target vascular plants and promote mild virulence.

Divergence of a genomic island leads to the evolution of melanization in a halophyte root fungus.

Understanding how organisms adapt to extreme living conditions is central to evolutionary biology. Dark septate endophytes (DSEs) constitute an important component of the root mycobiome and they are often able to alleviate host abiotic stresses. Here, we investigated the molecular mechanisms underlying the beneficial association between the DSE Laburnicola rhizohalophila and its host, the native halophyte Suaeda salsa, using population genomics. Based on genome-wide Fst (pairwise fixation index) and Vst analyses, which compared the variance in allele frequencies of single-nucleotide polymorphisms (SNPs) and copy number variants (CNVs), respectively, we found a high level of genetic differentiation between two populations. CNV patterns revealed population-specific expansions and contractions. Interestingly, we identified a ~20 kbp genomic island of high divergence with a strong sign of positive selection. This region contains a melanin-biosynthetic polyketide synthase gene cluster linked to six additional genes likely involved in biosynthesis, membrane trafficking, regulation, and localization of melanin. Differences in growth yield and melanin biosynthesis between the two populations grown under 2% NaCl stress suggested that this genomic island contributes to the observed differences in melanin accumulation. Our findings provide a better understanding of the genetic and evolutionary mechanisms underlying the adaptation to saline conditions of the L. rhizohalophila-S. salsa symbiosis.

Soil microbiome-mediated salinity tolerance in poplar plantlets is source-dependent.

Soil salinization is a global environmental problem and one of the most common land degradation processes. To effectively utilize saline lands, it is crucial to improve plant growth and stress tolerance, particularly through the microbiome intervention strategy. However, less is known about the interactions of microbes with trees than those with crops or herbaceous plants. Here, we examined how natural soil microbes affected the performance of salt-sensitive Populus deltoides × P. euramericana 'Nanlin895' (NL895) under salt stress. Gnotobiotic NL895 plantlets were inoculated with soil microbiome extracted from no-salt (NS; soluble salt: 0.71 g/kg), low-salt (LS; 5.14 g/kg), and high-salt (HS; 23.07 g/kg) lands, and then exposed to salt treatments. Compared to control, 33.8%, 18.0%, and 29.9% of the aboveground biomass was increased by NS, LS, and HS inoculation, respectively. The salt injury index was lower in LS and HS than in NS treatments. Rhizosphere microbial communities of all treatments were taxonomically and functionally different across multiple stages, while the variation extent was larger in bacterial than in fungal communities. FUNGuild and PICRUSt2 analysis demonstrated the changes of fungal trophic modes and bacterial metabolic pathways, respectively. In summary, our findings revealed the stronger potential of NS than LS and HS inoculants in growth promotion, while weaker strength than LS and HS inoculants in enhancing salt tolerance of NL895 plantlets. This source-dependent effect should be considered in future microbiome engineering, aiming at harnessing soil microbes to create predictable plant phenotypes.