Fungal communities represent the majority of root-specific transcripts in the transcriptomes of Agave plants grown in semiarid regions

Abstract

Agave plants present drought resistance mechanisms, commercial applications, and potential for bioenergy production. Currently, Agave species are used to produce alcoholic beverages and sisal fibers in semi-arid regions, mainly in Mexico and Brazil. Because of their high productivities, low lignin content, and high shoot-to-root ratio, agaves show potential as biomass feedstock to bioenergy production in marginal areas. Plants host many microorganisms and understanding their metabolism can inform biotechnological purposes. Here, we identify and characterize fungal transcripts found in three fiber-producing agave cultivars (Agave fourcroydes, A. sisalana, and hybrid 11648). We used leaf, stem, and root samples collected from the agave germplasm bank located in the state of Paraiba, in the Brazilian semiarid region, which has faced irregular precipitation periods. We used data from a de novo assembled transcriptome assembly (all tissues together). Regardless of the cultivar, around 10% of the transcripts mapped to fungi. Surprisingly, most root-specific transcripts were fungal (58%); of these around 64% were identified as Ascomycota and 28% as Basidiomycota in the three communities. Transcripts that code for heat shock proteins (HSPs) and enzymes involved in transport across the membrane in Ascomycota and Basidiomycota, abounded in libraries generated from the three cultivars. Indeed, among the most expressed transcripts, many were annotated as HSPs, which appear involved in abiotic stress resistance. Most HSPs expressed by Ascomycota are small HSPs, highly related to dealing with temperature stresses. Also, some KEGG pathways suggest interaction with the roots, related to transport to outside the cell, such as exosome (present in the three Ascomycota communities) and membrane trafficking, which were further investigated. We also found chitinases among secreted CAZymes, that can be related to pathogen control. We anticipate that our results can provide a starting point to the study of the potential uses of agaves’ fungi as biotechnological tools.

Molecular epidemiology of sisal bole rot disease suggests a potential phytosanitary crisis in Brazilian production areas

“…Also, cultivar interactions with sisal microbiome might be unique. Even though taxonomically similar microorganisms in A. sisalana and H11648 were found, transcriptomic analysis of these fungi revealed that the same groups might be using different metabolisms in each cultivar (Marone et al, 2022). The combination of these specific mechanisms may contribute to robust hybrids that simply make them healthier and, therefore, more able to deal with pathogenic microorganisms, such as A. welwitschiae.…”

Analysis of protein-protein interaction and weighted co-expression networks revealed key modules and genes in multiple organs of Agave sisalana

“…In addition, an enriched metabolic pathway of Plantpathogen interaction (ko04626; p.adjust = 0.00014) was identified, suggesting the presence of a phytopathogen. Recent studies using this same transcriptomic dataset have described several viral (Quintanilha-Peixoto et al, 2021) and fungal (Marone et al, 2022) interactions in A. sisalana, so this metabolic pathway might be a response to these interactions. Furthermore, the flavonoid biosynthesis pathway (ko00941; p.adjust = 0.03169) enrichment and the accumulation of these bioactive compounds in Agave species (Barriada-Bernal et al, 2014;Ahumada-Santos et al, 2013;Morreeuw et al, 2021) may indicate protection against these phytopathogens (Ferreyra.…”

Analysis of protein-protein interaction and weighted co-expression networks revealed key modules and genes in multiple tissues of Agave sisalana

“…In addition, an enriched metabolic pathway of Plant-pathogen interaction (ko04626; p.adjust=0.00014) was identi ed, suggesting the presence of a phytopathogen. Recent studies using this same transcriptomic dataset have described several viral (Quintanilha-Peixoto et al, 2021) and fungal (Marone et al, 2022) interactions in A. sisalana, so this metabolic pathway might be a response to these interactions. Also, Flavonoid biosynthesis (ko00941; p.adjust=0.03169) enriched may indicate the protection of A. sisalana against these phytopathogens (Falcone Ferreyra et al, 2012).…”

“…The GO enrichment of darkolivegreen module shows processes related to regulation of defense response to fungus, brassinosteroid biosynthetic process, and positive regulation of transcription initiation from RNA polymerase II promoter. Indeed, fungal transcripts were described in the same dataset (Marone et al, 2022). Although most fungal transcripts were root-speci c, some were present in the stem.…”