Characterization of Nonhost Resistance of Arabidopsis to the Asian Soybean Rust

Abstract

Asian soybean rust (ASR), caused by Phakopsora pachyrhizi, is a devastating disease of soybean. We report the use of the nonhost plant Arabidopsis thaliana to identify the genetic basis of resistance to P. pachyrhizi. Upon attack by P. pachyrhizi, epidermal cells of wild-type Arabidopsis accumulated H2O2, which likely orchestrates the frequently observed epidermal cell death. However, even when epidermal cell death occurred, fungal hyphae grew on and infection was terminated at the mesophyll boundary. These events were associated with expression of PDF1.2, suggesting that P. pachyrhizi, an ostensible biotroph, mimics aspects of a necrotroph. Extensive colonization of the mesophyll occurred in Arabidopsis pen mutants with defective penetration resistance. Although haustoria were found occasionally in mesophyll cells, the successful establishment of biotrophy failed, as evidenced by the cessation of fungal growth. Double mutants affected in either jasmonic acid or salicylic acid signaling in the pen3-1 background revealed the involvement of both pathways in nonhost resistance (NHR) of Arabidopsis to P. pachyrhizi. Interestingly, expression of AtNHL10, a gene that is expressed in tissue undergoing the hypersensitive response, was only triggered in infected pen3-1 mutants. Thus, a suppression of P. pachyrhizi-derived effectors by PEN3 can be inferred. Our results demonstrate that Arabidopsis can be used to study mechanisms of NHR to ASR.

Asian Soybean Rust – Meet a Prominent Challenge in Soybean Cultivation

“…We investigated for the first time the interaction between Arabidopsis and P. pachyrhizi in our lab and we started, therefore, with a detailed cytological analysis of the fungal infection process on wild-type Arabidopsis plants. Doing so, we observed that the fungus was not only able to penetrate epidermal cell walls but also grew further to the border of the mesopyll tissue where the infection process came to an end (Loehrer et al, 2008). Penetration of epidermal cells of nonhost plants was a known phenomenon for P. pachyrhizi (Hoppe and Koch, 1989).…”

“…It must be concluded, therefore, that P. pachyrhizi did not attack plants like a blind battering ram but rather utilizing subtle methods to cause cell death which might contribute to successful infection by avoiding active defense reactions. Looking at Arabidopsis mutant plants with impaired penetration resistance, we observed that after the breakdown of this first line of defense P. pachyrhizi w a s a b l e t o g r o w intercellularly into the mesophyll tissue and build haustorium mother cells (Loehrer et al, 2008). However, the pathogen was not able to invade mesophyll cells and establish haustorium-like structures until diminishing of a second line of defense in Arabidopsis pen2-1pad4-1 double mutants.…”

“…A recent example for this scenario is the occurrence of a novel pathogen species causing Asian soybean rust (Phakopsora pachyrhizi, Asian-Australian type) across the American continent which is more aggressive than the endogenous Latin-American species Phakopsora meibomiae. In an effort to identify novel sources for resistance against this pathogen we switched over to the plant model species Arabidopsis thaliana which shows complete resistance against the Asian soybean rust (Loehrer et al, 2008). This type of resistance is referred to as nonhost resistance and Arabidopsis is specifically suited to study this phenomenon because a whole range of different mutants is available which differ in their nonhost response to various pathogens (Thordal-Christensen, 2003).…”

“…As described above, nonhost resistance is displayed by a plant species against pathogens from other host plants and it is believed that this type of resistance is conditioned multifactorially and emerged in the course of evolution. We have tested a range of different Arabidopsis ecotypes collected all around the world for their response to inoculation with P. pachyrhizi and none of them showed disease symptoms or became infected (Loehrer et al, 2008). This result was taken as an indication that Arabidopsis and the Asian soybean rust indeed present a nonhost type of interaction.…”

“…These mutants are collectively called pen-mutants (penetration) and, so far, encompass three different genetic loci. While inoculation of pen1-1 and pen 2-1 mutants with P. pachyrhizi did not result in disease symptoms, pronounced necrotic spots were found on leaves of pen3-1 mutant plants (Loehrer et al, 2008). We further analysed the interaction of the pen-mutants with P. pachyrhizi by microscopy.…”