Entry Mode–Dependent Function of an Indole Glucosinolate Pathway in Arabidopsis for Nonhost Resistance against Anthracnose Pathogens

Abstract

When faced with nonadapted fungal pathogens, Arabidopsis thaliana mounts nonhost resistance responses, which typically result in the termination of early pathogenesis steps. We report that nonadapted anthracnose fungi engage two alternative entry modes during pathogenesis on leaves: turgor-mediated invasion beneath melanized appressoria, and a previously undiscovered hyphal tip-based entry (HTE) that is independent of appressorium formation. The frequency of HTE is positively regulated by carbohydrate nutrients and appears to be subject to constitutive inhibition by the fungal mitogenactivated protein kinase (MAPK) cascade of MAPK ESSENTIAL FOR APPRESSORIUM FORMATION1. The same MAPK cascade is essential for appressorium formation. Unexpectedly, the Arabidopsis indole glucosinolate pathway restricts entry of the nonadapted anthracnose fungi only when these pathogens employ HTE. Arabidopsis mutants defective in indole glucosinolate biosynthesis or metabolism support the initiation of postinvasion growth of nonadapted Colletotrichum gloeosporioides and Colletotrichum orbiculare. However, genetic disruption of Colletotrichum appressorium formation does not permit HTE on host plants. Thus, Colletotrichum appressoria play a critical role in the suppression of preinvasion plant defenses, in addition to their previously described role in turgor-mediated plant cell invasion. We also show that HTE is the predominant morphogenetic response of Colletotrichum at wound sites. This implies the existence of a fungal sensing system to trigger appropriate morphogenetic responses during pathogenesis at wound sites and on intact leaf tissue.

Leaf Oil Body Functions as a Subcellular Factory for the Production of a Phytoalexin in Arabidopsis

“…Infection-site defense strategies have been well characterized and work primarily to stop pathogen proliferation (Collins et al, 2003;Lipka et al, 2005;Jones and Dangl, 2006;Stein et al, 2006;Narusaka et al, 2009;Shirasu, 2009;Hiruma et al, 2010). This study shows that the perilesional tissues may also be involved in the prevention of fungal propagation through oil body-mediated toxin production.…”

“…They are responsible for the accumulation of stable phytoalexins in dead tissues and fallen leaves, which are unable to generate active defenses. Little is known about immunity in the perilesional area in plants, although immunity in the infected regions is well characterized (Collins et al, 2003;Hatsugai et al, 2004;Lipka et al, 2005;Jones and Dangl, 2006;Stein et al, 2006;Hatsugai et al, 2009;Narusaka et al, 2009;Shirasu, 2009;Hiruma et al, 2010;Hara-Nishimura and Hatsugai, 2011). This study provides a conceptual advance to our understanding of oil body function by revealing a form of perilesional defense in leaf oil bodies that is designed to block the spread of fungi from dead tissues to healthy tissues.…”

“…Colletotrichum lagenarium) strain 104-T (MAFF240422) were obtained from the MAFF GenBank. A transgenic C. higginsianum expressing RFP has been described previously (Hiruma et al, 2010). The fungal cultures were maintained on potato dextrose agar medium (Difco Laboratories) at 24°C in the dark.…”

“…An isolate of Colletotrichum higginsianum has been reported to infect Arabidopsis (Arabidopsis thaliana; Narusaka et al, 2004;O'Connell et al, 2004). The use of model plants enabled the characterization of the interaction between the fungus and Arabidopsis plants in the infected area (Narusaka et al, 2009;Hiruma et al, 2010Hiruma et al, , 2011. However, little is known about the defense responses in the perilesional area surrounding the infected area.…”

“…Experimental systems have been established using Colletotrichum species that consist of an infection assay, a conidia germination assay, and stable transformation procedures (Kimura et al, 2001;Takano et al, 2001;Hiruma et al, 2010). Recently, the genus Colletotrichum genome and transcriptome were analyzed (O'Connell et al, 2012).…”