Anti-Apoptotic Machinery Protects the Necrotrophic Fungus Botrytis cinerea from Host-Induced Apoptotic-Like Cell Death during Plant Infection

Abstract

Necrotrophic fungi are unable to occupy living plant cells. How such pathogens survive first contact with living host tissue and initiate infection is therefore unclear. Here, we show that the necrotrophic grey mold fungus Botrytis cinerea undergoes massive apoptotic-like programmed cell death (PCD) following germination on the host plant. Manipulation of an anti-apoptotic gene BcBIR1 modified fungal response to PCD-inducing conditions. As a consequence, strains with reduced sensitivity to PCD were hyper virulent, while strains in which PCD was over-stimulated showed reduced pathogenicity. Similarly, reduced levels of PCD in the fungus were recorded following infection of Arabidopsis mutants that show enhanced susceptibility to B. cinerea. When considered together, these results suggest that Botrytis PCD machinery is targeted by plant defense molecules, and that the fungal anti-apoptotic machinery is essential for overcoming this host-induced PCD and hence, for establishment of infection. As such, fungal PCD machinery represents a novel target for fungicides and antifungal drugs.

Plastic Transcriptomes Stabilize Immunity to Pathogen Diversity: The Jasmonic Acid and Salicylic Acid Networks within the Arabidopsis/Botrytis Pathosystem

“…This suggests that this collection of B. cinerea genotypes does not contain large-effect qualitative virulence loci; instead, this generalist uses a highly polygenic virulence architecture (Denby et al, 2004;Finkers et al, 2007b;Rowe and Kliebenstein, 2008;Corwin et al, 2016b;Zhang et al, 2016). This agrees with previous B. cinerea mechanistic studies that identify a large collection of standing genetic variation that controls a wide range of specific virulence mechanisms (Choquer et al, 2007;Rowe and Kliebenstein, 2007;Noda et al, 2010;Rowe et al, 2010;Dalmais et al, 2011;Michielse et al, 2011;Shlezinger et al, 2011;Windram et al, 2012;Pearson and Bailey, 2013;Kumari et al, 2014;An et al, 2015;Atwell et al, 2015;Hevia et al, 2015;Plaza et al, 2015;Schumacher et al, 2015;Zhang et al, 2015a;Corwin et al, 2016aCorwin et al, , 2016bLopezCruz et al, 2017;Zhang et al, 2016). Taken together, this supports the perspective that the Arabidopsis-B.…”

Involvement of Botrytis cinerea Small GTPases BcRAS1 and BcRAC in Differentiation, Virulence, and the Cell Cycle

“…While the mechanism behind this phenomenon has yet to be resolved, it points to defects in the coordination of pathogenic development at both early and late infection phases. According to a working model proposed by Shlezinger and coworkers (34), B. cinerea first secretes necrosisinducing compounds that mediate the early infection stage, and then the fungus produces programmed cell death (PCD)-inducing factors that mediate the spreading lesion. It is possible that regulation of these events is disrupted in the CA-BcRAC strain such that it produces larger amounts of necrosis-inducing factors (e.g., necrosis-inducing proteins or ROS) during the first hours p.i., but the transition between the early and late infection phases and secretion of PCD-inducing factors is delayed.…”

“…These results indicated that the CABcRAC strain is altered in early stages of pathogenic development. The initial acceleration of lesion formation could be due to enhanced secretion of necrotizing agents, whereas the pause in development at 48 h is suggestive of defects in the transition from early to late infection phases (34).…”

Role of Phytoalexins in Plant Disease Resistance

“…Conidia of B. cinerea showed a complete disorganization of mitochondria and disruption of the plasma membrane upon treatment with the stilbene phytoalexins, resveratrol and pterostilbene. Camalexin has recently been involved in the induction of fungal apoptotic programmed cell death in B. cinerea (Shlezinger et al, 2011). The efficaciousness in vivo of some phytoalexins, namely the coumarin phytoalexin, scopoletin on the reduction of green mold symptoms caused by Penicillium digitatum on oranges was shown (Sanzani et al,, 2014).…”