Early Responses in the Arabidopsis-Verticillium longisporum Pathosystem Are Dependent on NDR1, JA- and ET-Associated Signals via Cytosolic NPR1 and RFO1

Abstract

The responses of Arabidopsis accessions and characterized genotypes were used to explore components in the early defense responses to the soilborne fungus Verticillium longisporum. V. longisporum susceptibility was found to be a complex trait, in which different disease phenotypes, such as stunting, altered flowering time, weight loss, and chlorosis were perceived differently across genotypes. A Bay-0 x Shahdara recombinant inbred line population was used to identify two loci on chromosomes 2 and 3 of Bay-0 origin that caused enhanced chlorosis after V. longisporum challenge. Furthermore, the observation that a mutation in RFO1 in Col-0 resulted in susceptibility whereas the natural rfo1 allele in Ty-0 showed a high degree of resistance to the pathogen supports the hypothesis that several resistance quantitative trait loci reside among Arabidopsis accessions. Analysis of mutants impaired in known pathogen response pathways revealed an enhanced susceptibility in ein2-1, ein4-1, ein6-1, esa1-1, and pad1-1, but not in other jasmonic acid (JA)-, ethylene (ET)-, or camalexin-deficient mutants, suggesting that V. longisporum resistance is regulated via a hitherto unknown JA- and ET-associated pathway. Pretreatments with the ET precursor 1-aminocyclo-propane-1-carboxylic acid (ACC) or methyl jasmonate (MeJA) caused enhanced resistance to V. longisporum. Mutants in the salicylic acid (SA) pathway (eds1-1, NahG, npr1-3, pad4-1, and sid2-1) did not show enhanced susceptibility to V. longisporum. In contrast, the more severe npr1-1 allele displayed enhanced V. longisporum susceptibility and decreased responses to ACC or MeJA pretreatments. This shows that cytosolic NPR1, in addition to SA responses, is required for JA- and ET-mediated V. longisporum resistance. Expression of the SA-dependent PR-1 and PR-2 and the ET-dependent PR-4 were increased 7 days postinoculation with V. longisporum. This indicates increased levels of SA and ET in response to V. longisporum inoculation. The R-gene signaling mutant ndr1-1 was found to be susceptible to V. longisporum, which could be complemented by ACC or MeJA pretreatments, in contrast to the rfo1 T-DNA mutant, which remained susceptible, suggesting that RFO1 (Fusarium oxysporum resistance) and NDR1 (nonrace specific disease resistance 1) activate two distinct signaling pathways for V. longisporum resistance.

Fusarium oxysporum hijacks COI1‐mediated jasmonate signaling to promote disease development in Arabidopsis

“…However, coi1 also displays enhanced susceptibility to the soil-borne oomycete pathogens Pythium irregulare (Adie et al, 2007) and Pythium mastophorum (Vijayan et al, 1998), as well as the vascular wilt-inciting fungal pathogen Verticillium longispo- rum (Johansson et al, 2006), suggesting that the effect of the coi1 mutation in restricting disease symptom development is more specific to F. oxysporum. Interestingly, coi1 also exhibited reduced susceptibility to the soil-borne bacterial wilt pathogen Ralstonia solanacearum (Hernandez-Blanco et al, 2007), and to root-knot nematodes (Meloidogyne spp.)…”

The Vascular Pathogen Verticillium longisporum Requires a Jasmonic Acid-Independent COI1 Function in Roots to Elicit Disease Symptoms in Arabidopsis Shoots

“…Due to the growing demand for oil crops as sources for nutritional oils and biofuels, novel strategies to limit the spread of V. longisporum are needed. Since these can be based on the molecular mechanisms of defense responses, several groups have started to investigate the interaction between V. longisporum and the model plant Arabidopsis (Steventon et al, 2001;Veronese et al, 2003;Johansson et al, 2006;Floerl et al, 2010Floerl et al, , 2012.…”

Análisis genético de la percepción del ácido salicílico en Arabidopsis thaliana. Caracterización de NRB4

“…In contrast, the npr1-1 mutant, which has a mutation in a key domain, is affected in the expression of SA, JA and ET-dependent genes (Glazebrook et al 2003). More recent studies support such cytosolic NPR1 function as regulator of JAdependent defense responses (Johansson et al 2006;Leon-Reyes et al 2009;Ramirez et al 2010). …”

“…ISR, (Pieterse et al 1998); Verticilium resistance, (Johansson et al 2006); resistance induced by Piriformospora indica, (Stein et al 2008); etc.) remains to be assessed.…”

“…En el caso de la inducción de resistencia tras la aplicación de MeJA (también conocida como MIR), nuevamente se ha postulado al gen NPR1 como relevante (Pieterse et al 1998), aunque su función en este proceso aún no ha sido bien definida. No obstante, estudios posteriores han sugerido que la forma citosólica de la proteína estaría implicada en la regulación de las respuestas defensivas dependientes del JA (Glazebrook et al 2003;Johansson et al 2006;Ramirez et al 2010). Estos estudios se han basado en las diferencias existentes entre dos de los mutantes descritos: npr1-1 y npr1-3 (Cao et al 1997).…”