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Deciphering common and specific transcriptional immune responses in pea towards the oomycete pathogens Aphanomyces euteiches and Phytophthora pisi.

ABSTRACT: Root rot caused by Aphanomyces euteiches is one of the most destructive pea diseases while a distantly related species P. pisi has been recently described as the agent of pea and faba bean root rot. These two oomycete pathogens with different pathogenicity factor repertories have both evolved specific mechanisms to infect pea. However, little is known about the genes and mechanisms of defence against these pathogens in pea. In the present study, the transcriptomic response of pea to these two pathogens was investigated at two time points during early phase of infection using a Medicago truncatula microarray.Of the 37,976 genes analysed, 574 and 817 were differentially expressed in response to A. euteiches at 6 hpi and 20 hpi, respectively, while 544 and 611 genes were differentially regulated against P. pisi at 6 hpi and 20 hpi, respectively. Differentially expressed genes associated with plant immunity responses were involved in cell wall reinforcement, hormonal signalling and phenylpropanoid metabolism. Activation of cell wall modification, regulation of jasmonic acid biosynthesis and induction of ethylene signalling pathway were among the common transcriptional responses to both of these oomycetes. However, induction of chalcone synthesis and the auxin pathway were specific transcriptional changes against A. euteiches.Our results demonstrate a global view of differentially expressed pea genes during compatible interactions with P. pisi and A. euteiches at an early phase of infection. The results suggest that distinct signalling pathways are triggered in pea by these two pathogens that lead to common and specific immune mechanisms in response to these two oomycetes. The generated knowledge may eventually be used in breeding pea varieties with resistance against root rot disease.

SUBMITTER: Hosseini S

PROVIDER: S-EPMC4546216 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Deciphering common and specific transcriptional immune responses in pea towards the oomycete pathogens Aphanomyces euteiches and Phytophthora pisi.

Hosseini Sara S Elfstrand Malin M Heyman Fredrik F Funck Jensen Dan D Karlsson Magnus M

BMC genomics 20150821

<h4>Background</h4>Root rot caused by Aphanomyces euteiches is one of the most destructive pea diseases while a distantly related species P. pisi has been recently described as the agent of pea and faba bean root rot. These two oomycete pathogens with different pathogenicity factor repertories have both evolved specific mechanisms to infect pea. However, little is known about the genes and mechanisms of defence against these pathogens in pea. In the present study, the transcriptomic response of ...[more]

PMID: 26293353

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Project description:Combining plant genetic resistance with architectural traits that are unfavorable to disease development is a promising strategy for reducing epidemics. However, few studies have identified root system architecture (RSA) traits with the potential to limit root disease development. Pea is a major cultivated legume worldwide and has a wide level of natural genetic variability for plant architecture. The root pathogen Aphanomyces euteiches is a major limiting factor of pea crop yield. This study aimed to increase the knowledge on the diversity of loci and candidate genes controlling RSA traits in pea and identify RSA genetic loci associated with resistance to A. euteiches which could be combined with resistance QTL in breeding. A comparative genome wide association (GWA) study of plant architecture and resistance to A. euteiches was conducted at the young plant stage in a collection of 266 pea lines contrasted for both traits. The collection was genotyped using 14,157 SNP markers from recent pea genomic resources. It was phenotyped for ten root, shoot and overall plant architecture traits, as well as three disease resistance traits in controlled conditions, using image analysis. We identified a total of 75 short-size genomic intervals significantly associated with plant architecture and overlapping with 46 previously detected QTL. The major consistent intervals included plant shoot architecture or flowering genes (PsLE, PsTFL1) with putative pleiotropic effects on root architecture. A total of 11 genomic intervals were significantly associated with resistance to A. euteiches confirming several consistent previously identified major QTL. One significant SNP, mapped to the major QTL Ae-Ps7.6, was associated with both resistance and RSA traits. At this marker, the resistance-enhancing allele was associated with an increased total root projected area, in accordance with the correlation observed between resistance and larger root systems in the collection. Seven additional intervals associated with plant architecture overlapped with GWA intervals previously identified for resistance to A. euteiches. This study provides innovative results about genetic interdependency of root disease resistance and RSA inheritance. It identifies pea lines, QTL, closely-linked markers and candidate genes for marker-assisted-selection of RSA loci to reduce Aphanomyces root rot severity in future pea varieties.

Project description:Aphanomyces euteiches is an oomycete pathogen with a broad host-range on legumes that causes devastating root rot disease in many pea-growing countries and especially in France. Genetic resistance is a promising way to manage the disease since consistent QTL controlling partial resistance have been identified in near isogenic lines of pea. However, there are still no resistant pea varieties cultivated in France. This study aimed to evaluate the phenotypic and genetic diversity of A. euteiches populations from the major pea-growing regions in France. A collection of 205 isolates, from soil samples collected in infested pea fields located in five French regions, was established and genotyped using 20 SSR markers. Thirteen multilocus genotypes were found among the 205 isolates which displayed a low genotypic richness (ranged from 0 to 0.333). Two main clusters of isolates were identified using PCoA and STRUCTURE, including a predominant group comprising 88% of isolates and another group representing 12% of isolates mainly from the Bourgogne region. A subset of 34 isolates, representative of the fields sampled, was phenotyped for aggressiveness on a set of resistant and susceptible varieties of four legume hosts (pea, faba bean, vetch, alfalfa). Significant differences in disease severity were found among isolates and three groups of aggressiveness comprising 16, 17, and 2 isolates, respectively, were identified using HCA analysis. A higher diversity in pathogen aggressiveness was observed among isolates from Bourgogne, which included different legumes in its crop history. Little relationship was observed between genetic clusters and pathogenicity in the subset of 34 isolates, as expected using neutral markers. This study provides useful knowledge on the current state of low to moderate diversity among A. euteiches populations before resistant pea varieties are grown in France. New insights and hypotheses about the major factors shaping the diversity and evolution of A. euteiches are also discussed.

Project description:The cultivation of vining pea (Pisum sativum) faces a major constraint with root rot diseases, caused by a complex of soil-borne pathogens including the oomycetes Aphanomyces euteiches and Phytophtora pisi. Disease resistant commercial varieties are lacking but the landrace PI180693 is used as a source of partial resistance in ongoing pea breeding programs. In this study, the level of resistance and their interaction with A. euteiches virulence levels of six new back-crossed pea breeding lines, deriving from the cross between the susceptible commercial cultivar Linnea and PI180693, were evaluated for their resistance towards aphanomyces root rot in growth chamber and green house tests. Resistance towards mixed infections by A. euteiches and P. pisi and commercial production traits were evaluated in field trials. In growth chamber trials, pathogen virulence levels had a significant effect on plant resistance, as resistance was more consistent against A. euteiches strains exhibiting high or intermediate virulence compared with lowly virulent strains. In fact, line Z1701-1 showed to be significantly more resistant than both parents when inoculated with a lowly virulent strain. In two separate field trials in 2020, all six breeding lines performed equally well as the resistant parent PI180693 at sites only containing A. euteiches, as there were no differences in disease index. In mixed infections, PI180693 exhibited significantly lower disease index scores than Linnea. However, breeding lines displayed higher disease index scores compared with PI180693, indicating higher susceptibility towards P. pisi. Data on seedling emergence from the same field trials suggested that PI180693 was particularly sensitive towards seed decay/damping off disease caused by P. pisi. Furthermore, the breeding lines performed equally well as Linnea in traits important for green pea production, again emphasizing the commercial potential. In summary, we show that the resistance from PI180693 interacts with virulence levels of the pathogen A. euteiches and is less effective towards root rot caused by P. pisi. Our results show the potential use of combining PI180693 partial resistance against aphanomyces root rot with commercially favorable breeding traits in commercial breeding programs.

Dataset Information

Deciphering common and specific transcriptional immune responses in pea towards the oomycete pathogens Aphanomyces euteiches and Phytophthora pisi.

Publications

Deciphering common and specific transcriptional immune responses in pea towards the oomycete pathogens Aphanomyces euteiches and Phytophthora pisi.

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