Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica

Abstract

Recent sequencing projects have provided deep insight into fungal lifestyle-associated genomic adaptations. Here we report on the 25 Mb genome of the mutualistic root symbiont Piriformospora indica (Sebacinales, Basidiomycota) and provide a global characterization of fungal transcriptional responses associated with the colonization of living and dead barley roots. Extensive comparative analysis of the P. indica genome with other Basidiomycota and Ascomycota fungi that have diverse lifestyle strategies identified features typically associated with both, biotrophism and saprotrophism. The tightly controlled expression of the lifestyle-associated gene sets during the onset of the symbiosis, revealed by microarray analysis, argues for a biphasic root colonization strategy of P. indica. This is supported by a cytological study that shows an early biotrophic growth followed by a cell death-associated phase. About 10% of the fungal genes induced during the biotrophic colonization encoded putative small secreted proteins (SSP), including several lectin-like proteins and members of a P. indica-specific gene family (DELD) with a conserved novel seven-amino acids motif at the C-terminus. Similar to effectors found in other filamentous organisms, the occurrence of the DELDs correlated with the presence of transposable elements in gene-poor repeat-rich regions of the genome. This is the first in depth genomic study describing a mutualistic symbiont with a biphasic lifestyle. Our findings provide a significant advance in understanding development of biotrophic plant symbionts and suggest a series of incremental shifts along the continuum from saprotrophy towards biotrophy in the evolution of mycorrhizal association from decomposer fungi.

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

“…A first analysis of the distribution on a world-wide scale claimed that Sebacinalean symbioses are prevalent in all continents (Weiss et al, 2011;Riess et al, 2014) potentially making them a vital part of global soil ecosystems. Although the molecular mechanisms by which the Sebacinalean symbiosis is established and by which the plant benefits from its fungal partners is largely understood, the role of the endofungal bacteria is still unclear (Peškan-Berghöfer et al, 2004;Waller et al, 2005;Deshmukh et al, 2006;Camehl et al, 2010;Zuccaro et al, 2011;Qiang et al, 2012b).…”

Phosphate utilization by the fungal root endophyte Piriformospora indica

“…Citrate, oxalate and malate are discussed to be involved in phosphate solubilisation in the rhizosphere (Jones 1998). No genes encoding an oxalate synthase could be detected in the genome of P. indica, but one gene for a malate synthase and three genes for a citrate synthase have been identified (Zuccaro et al 2011). All four genes are mainly expressed when P. indica is cultivated without the plant, which suggests that these fungal enzymes are needed for solubilising nutrients (Zuccaro et al 2011).…”

“…To clarify whether the results for phytase and phosphatase activity can be explained by P. indica genome composition, the database published by Zuccaro et al (2011) was screened for the corresponding genes. For both activities each two full size genes could be detected which were called PiPHY1, PiPHY2, PiAPH1 and PiAPH2 (Table S1).…”

“…Based on the genomic information (Zuccaro et al 2011), we found that P. indica has the potential to express four different phosphate transporters, two acid phosphatases and two phytases. Although two genes encoding acid phosphatases and two phytase genes were expressed under our conditions, neither intra-nor extracellular enzymatic activity was detected in comparison with the reaction of our positive control.…”

Identification of Plasmodiophora brassicae effectors — A challenging goal

“…Computational prediction is an excellent starting point to screen for putative effectors, to identify functional domains and to help us understand the evolution, distribution and characteristics of effectors [75,76]. Utilizing the information presented in this review we have designed a coherent pipeline aimed at identifying putative effectors involved in the infection process by P. brassicae and subsequent clubroot disease progression in its plant host (Figure 2).…”