Transcriptomic changes in the plant pathogenic fungus Rhizoctonia solani AG-3 in response to the antagonistic bacteria Serratia proteamaculans and Serratia plymuthica

Abstract

BackgroundImproved understanding of bacterial-fungal interactions in the rhizosphere should assist in the successful application of bacteria as biological control agents against fungal pathogens of plants, providing alternatives to chemicals in sustainable agriculture. Rhizoctonia solani is an important soil-associated fungal pathogen and its chemical treatment is not feasible or economic. The genomes of the plant-associated bacteria Serratia proteamaculans S4 and Serratia plymuthica AS13 have been sequenced, revealing genetic traits that may explain their diverse plant growth promoting activities and antagonistic interactions with R. solani. To understand the functional response of this pathogen to different bacteria and to elucidate whether the molecular mechanisms that the fungus exploits involve general stress or more specific responses, we performed a global transcriptome profiling of R. solani Rhs1AP anastomosis group 3 (AG-3) during interaction with the S4 and AS13 species of Serratia using RNA-seq.ResultsApproximately 104,504 million clean 75-100 bp paired-end reads were obtained from three libraries, each in triplicate (AG3-Control, AG3-S4 and AG3-AS13). Transcriptome analysis revealed that approximately 10 % of the fungal transcriptome was differentially expressed during challenge with Serratia. The numbers of S4- and AS13-specific differentially expressed genes (DEG) were 866 and 292 respectively, while there were 1035 common DEGs in the two treatment groups. Four hundred and sixty and 242 genes respectively had values of log2 fold-change > 3 and for further analyses this cut-off value was used. Functional classification of DEGs based on Gene Ontology enrichment analysis and on KEGG pathway annotations revealed a general shift in fungal gene expression in which genes related to xenobiotic degradation, toxin and antioxidant production, energy, carbohydrate and lipid metabolism and hyphal rearrangements were subjected to transcriptional regulation.ConclusionsThis RNA-seq profiling generated a novel dataset describing the functional response of the phytopathogen R. solani AG3 to the plant-associated Serratia bacteria S4 and AS13. Most genes were regulated in the same way in the presence of both bacterial isolates, but there were also some strain-specific responses. The findings in this study will be beneficial for further research on biological control and in depth exploration of bacterial-fungal interactions in the rhizosphere.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1758-z) contains supplementary material, which is available to authorized users.

Transcriptomic responses of a simplified soil microcosm to a plant pathogen and its biocontrol agent reveal a complex reaction to harsh habitat

“…Soil microorganisms are key determinants of biological soil quality, supporting soil fertility and indirectly plant health [1]. Soil bacteria and fungi have undergone evolution and niche differentiation, interacting in different ways with various outcomes in soil ecosystems [2]. Microbe-microbe interactions have an important impact on microbial fitness in the soil [3] and they can positively or negatively affect other participants, including organisms of higher taxa [4].…”

“…Molecular interplay between soil microorganisms has mainly been studied in dual cultures of plant pathogens and biocontrol agents [2, 7–10]. Soil phytopathogenic fungi cause severe diseases in several crops, and Armillaria spp.…”

“…have been extensively studied using several approaches, including transcriptomics [17]. Most transcriptomic studies of microbial biocontrol mechanisms have focused on molecular responses of the biocontrol agent and the target plant pathogen in dual cultures [2, 7, 8, 10, 18]. However, microbial properties in complex consortia often differ from those of their single components [19].…”

Leuconostoc spp. Associated with Root Rot in Sugar Beet and Their Interaction with Rhizoctonia solani

“…and R. solani. Other investigations studying R. solani on sugar beet and other crops have been focused on investigating bacteria in an effort to develop a biocontrol to limit disease development by the fungus (De Curtis et al 2010;Gkarmiri et al 2015;Heydari and Misaghi 2003;Hua and Höfte 2015;Lovic et al 1993;Mendes et al 2011;Olorunleke et al 2015;Postma and Schilder 2015;Postma et al 2010;Schillinger and Paulitz 2014;Solanki et al 2012;Weller et al 2002;Yin et al 2013;Zachow et al 2011).…”

Comments on bacterial and fungal interactions in medicine, agriculture and the environment

“…Microfluidic devices have provided the latitude for microscopic research, long-run and time-lapse studies (Stanley et al, 2014). Elucidation of bacterial-fungal interactions in the rhizosphere is liable to enhance the feasible bacterial application to curb plant fungal pathogens as alternatives to chemicals in sustainable agriculture (Gkarmiri et al, 2015, Chukwuma, 2014, as well as full and proper elucidation of biochemical processes and biosynthetic pathways (Chukwuma 2016b, c;Chukwuma, 2017).…”