Upgrading Root Physiology for Stress Tolerance by Ectomycorrhizas: Insights from Metabolite and Transcriptional Profiling into Reprogramming for Stress Anticipation

Abstract

Ectomycorrhizas (EMs) alleviate stress tolerance of host plants, but the underlying molecular mechanisms are unknown. To elucidate the basis of EM-induced physiological changes and their involvement in stress adaptation, we investigated metabolic and transcriptional profiles in EM and non-EM roots of gray poplar (Populus 3 canescens) in the presence and absence of osmotic stress imposed by excess salinity. Colonization with the ectomycorrhizal fungus Paxillus involutus increased root cell volumes, a response associated with carbohydrate accumulation. The stress-related hormones abscisic acid and salicylic acid were increased, whereas jasmonic acid and auxin were decreased in EM compared with non-EM roots. Auxin-responsive reporter plants showed that auxin decreased in the vascular system. The phytohormone changes in EMs are in contrast to those in arbuscular mycorrhizas, suggesting that EMs and arbuscular mycorrhizas recruit different signaling pathways to influence plant stress responses. Transcriptome analyses on a whole genome poplar microarray revealed activation of genes related to abiotic and biotic stress responses as well as of genes involved in vesicle trafficking and suppression of auxin-related pathways. Comparative transcriptome analysis indicated EM-related genes whose transcript abundances were independent of salt stress and a set of salt stress-related genes that were common to EM non-salt-stressed and non-EM salt-stressed plants. Salt-exposed EM roots showed stronger accumulation of myoinositol, abscisic acid, and salicylic acid and higher K + -to-Na + ratio than stressed non-EM roots. In conclusion, EMs activated stress-related genes and signaling pathways, apparently leading to priming of pathways conferring abiotic stress tolerance.Under natural conditions, many economically important tree species including fast-growing poplars (Populus spp.) form ectomycorrhizas (EMs) between roots and EM fungi. Colonization with EM fungi leads to profound changes in root architecture and morphology. Usually, EM roots are strongly ramnified and EM root tips show a bulb-like appearance (Smith and Read, 2008). In EMs, plants and fungi interact mutualistically: while the plant receives mineral nutrients and water through the fungus, the fungus is supplied with carbohydrates by its host (Smith and Read, 2008). To fulfill these functions, specific anatomical structures are established, which involve the formation of a hyphal mantle ensheathing the root tip with hyphae emanating into soil for nutrient uptake. Inside the mantle, hyphae grow between, but not inside, the cortex cells within the cell wall, forming an interface called the Hartig net for bidirectional nutrient exchange.The establishment of EMs requires a coordinated developmental program in both partners of the symbiosis. Transcriptional changes during initial stages of host recognition and colonization have been the focus of several recent studies (Johansson et al., 2004;Duplessis et al., 2005;Le Queré et al., 2005;Morel et

Linking the Salt Transcriptome with Physiological Responses of a Salt-Resistant Populus Species as a Strategy to Identify Genes Important for Stress Acclimation

“…Salt exposure generally leads to increased abscisic acid levels, but in Euphrat poplar more rapidly than in salt-sensitive poplar species (Chen et al, 2001;Luo et al, 2009). Here, activation of a putative homeodomain transcription factor (homolog to ATHB-7) and aldehyde dehydrogenase was observed, which are known to be regulated by abscisic acid and to be responsive to salinity and drought (Sö derman et al, 1996;Seki et al, 2002;Olsson et al, 2004;Sunkar et al, 2003;Kotchoni et al, 2006).…”

“…We used loss-of-function mutants of Arabidopsis to test the involvement of TIL and SIS, a salt-regulated unknown gene in salt tolerance. Data mining showed that SIS expression was typically regulated by salt treatment (Kilian et al, 2007;Luo et al, 2009). We show that suppression of its expression renders Arabidopsis knockout mutants more salt susceptible.…”

Plant Metabolomics: A Characterisation of Plant Responses to Abiotic Stresses

“…In agreement with the metabolic data, a microarray analysis indicated a constitutive activation of stress-related genes in control EM-roots, that are activated by salt stress in non-EM roots. Altogether, the data of Luo et al (2009) indicated a stronger induction of defence pathways and metabolites in EM roots than in non-EM roots exposed to excess salinity, suggesting that the fungus P. involutus was able to prime the poplar plants for increased stress tolerance.…”

“…Most of the knowledge on the improved stress protection comes from plants interacting with arbuscular mycorrhizas (AMs), whereas relatively little information is available on molecular and physiological mechanisms underlying the enhancement of stress tolerance in host plants by ectomycorrhizas (EMs). Luo et al (2009) have investigated the transcriptional and metabolic profiles in EM and non-EM roots of gray poplar (Populus x canescens) under control or excess-salinity conditions. The mycelia of the fungus Paxillus involutus were used for mycorrhizal inoculation.…”

Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes

“…Pathogens, such as P. syringae and H. arabidopsidis, attempt to manipulate the plant response by producing effectors that target different components of the JA (i.e., JAZ proteins) and ET signaling pathways (i.e., ERF proteins) in such a fashion that colonization is favored (10,11,23,24). Like pathogenic bacteria, mutualistic fungi affect plant hormone signaling cascades to achieve colonization (31)(32)(33)(34)(35), although the knowledge of the mechanistic reasoning behind most of these differences is in its infancy. We demonstrate here that MiSSP7, an effector protein produced by 0013s07840 0092s00200 0001s31570 0013s04880 0001s36520 0001s21010 0015s15750 0015s15730 0003s21660 0017s01230 0019s14550 0001s01010 0001s22610 0010s25380 0001s23460 0014s12130 0002s20290 0002s17750 0014s12100 0001s23440 0015s13190 (29), in roots treated with 10 −8 M MeJA (white bars), in two independent transgenic lines expressing MiSSP7 (gray and black bars) and in roots colonized by L. bicolor (stippled bars).…”