Plant pathogenic and beneficial fungi have evolved several strategies to evade immunity and cope with host-derived hydrolytic enzymes and oxidative stress in the apoplast, the extracellular space of plant tissues. Fungal hyphae are surrounded by an inner insoluble cell wall (CW) layer and an outer soluble extracellular polysaccharide (EPS) matrix. Here we show by proteomics and glycomics that these two layers have distinct protein and carbohydrate signatures, and hence likely have different biological functions. The barley (Hordeum vulgare) β-1,3-endoglucanase HvBGLUII, which belongs to the widely distributed apoplastic glycoside hydrolase 17 family (GH17), releases a conserved β-1,3;1,6-glucan decasaccharide (β-GD) from the EPS matrices of fungi with different lifestyles and taxonomic positions. This low molecular weight β-GD does not activate plant immunity, is resilient to further enzymatic hydrolysis by β-1,3-endoglucanases due to the presence of three β-1,6-linked glucose branches and can scavenge reactive oxygen species. Exogenous application of β-GD leads to enhanced fungal colonization in barley, confirming its role in the fungal counterdefensive strategy to subvert host immunity. Our data highlight the hitherto undescribed capacity of this often-overlooked EPS matrix from plant-associated fungi to act as an outer protective barrier important for fungal accommodation within the hostile environment at the apoplastic plant-microbe interface.
Dioecy, the separation of reproductive organs on different individuals, has evolved repeatedly in different plant families. Several evolutionary paths to dioecy have been suggested, but the mechanisms behind sex determination is not well understood. The diploid dioecious Amaranthus palmeri represents a well-suited model system to study sex determination in plants. Despite the agricultural importance of the species, the genetic control and evolutionary state of dioecy in A. palmeri is currently unknown. Early cytogenetic experiments did not identify heteromorphic chromosomes. Here, we used whole-genome sequencing of male and female pools from 2 independent populations to elucidate the genetic control of dioecy in A. palmeri. Read alignment to a close monoecious relative and allele frequency comparisons between male and female pools did not reveal significant sex-linked genes. Consequently, we employed an alignment-free k-mer comparison which enabled us to identify a large number of male-specific k-mers. We assembled male-specific contigs comprising a total of almost 2 Mb sequence, proposing a XY sex-determination system in the species. We were able to identify the potential Y chromosome in the A. palmeri draft genome sequence as 90% of our male-specific sequence aligned to a single scaffold. Based on our findings, we suggest an intermediate evolutionary state of dioecy with a young Y chromosome in A. palmeri. Our findings give insight into the evolution of sex chromosomes in plants and may help to develop sustainable strategies for weed management.
Dioecy, the separation of reproductive organs on different individuals, has evolved repeatedly in different plant families. Several evolutionary paths to dioecy have been suggested, but the mechanisms behind sex determination is not well understood. The diploid dioecious Amaranthus palmeri represents a well suited model system to study sex determination in plants. A. palmeri is one of the most troublesome weeds in the US, has successfully colonized other regions in the world and has evolved resistance to several herbicide classes. Despite the agricultural importance of the species, the genetic control and evolutionary state of dioecy in A. palmeri is currently unknown. Early cytogenetic experiments did not identify heteromorphic chromosomes. Here, we used whole genome sequencing of male and female pools from two independent populations to elucidate the genetic control of dioecy in A. palmeri. Read alignment to a close monoecious relative and allele frequency comparisons between male and female pools did not reveal significant sex linked genes. Consequently, we employed an alignment free k-mer comparison which enabled us to identify a large number of male specific k-mers. We assembled male specific contigs comprising a total of almost 2 Mb sequence, proposing a XY sex determination system in the species. Based on our findings we suggest an intermediate evolutionary state of dioecy in A. palmeri. Our findings give insight into the evolution of sex chromosomes in plants and may help to develop sustainable strategies for weed management.
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