Plant Science 233 (2015) 53–60 Contents lists available at ScienceDirect Plant Science j ourna l ho me pa ge: www.elsevier.com/locate/plantsci Review Pathogenic attributes of Sclerotinia sclerotiorum: Switching from a biotrophic to necrotrophic lifestyle Mehdi Kabbage a,1 , Oded Yarden b,1 , Martin B. Dickman c,d,* a Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI, USA b Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 7600, Israel c Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, TX, USA d Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA a r t i c l e i n f o Article history: Received 10 October 2014 Received in revised form 20 December 2014 Accepted 22 December 2014 Available online 31 December 2014 Keywords: Fungal pathogens Necrotrophy Biotrophy Lifestyle designations Sclerotinia sclerotiorum Damage curve a b s t r a c t Plants and fungi have had many years of friendly and not-so friendly competition for resources and qual- ity of life. As a result, diverse pathosystems evolved numerous strategies, coupled with the emergence of multifaceted pathogenic and saprophytic lifestyles. We discuss fungal lifestyle classifications and how the views associated with certain fungal pathogens, particularly necrotophs, are changing as we learn more about the complexities of their interactions with a given host plant. We discuss the physiological events leading to the transition from biotrophy to necrotrophy in hemi-biotrophs, and conclude that both the control of plant immune responses and the need for a more efficient mode of nutrient acquisition are possible triggers for the transition to necrotrophy. Based on recent findings, we focus on the polyphagous plant pathogen Sclerotinia sclerotiorum. Rather than overwhelming plant foes, S. sclerotiorum has evolved clever means to compromise host recognition and establish disease, resulting in a broad and immensely successful pathogenic lifestyle. The tactics used by this fungus to achieve pathogenic success are being clarified. We propose that the hemi-biotrophic lifestyle may be more temporally and spatially complex than currently depicted, and that combining lifestyle attributes with damage response curves that con- sider the contribution of both the fungus and the host to pathogenesis, may provide a more holistic manner to view plant pathogens. © 2015 Published by Elsevier Ireland Ltd. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 1.1. Cell wall degrading capacity and fungal lifestyles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54 1.2. Are effectors determinants of biotrophy? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54 1.3. Lifestyle designation of S. sclerotiorum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54 2. Why do hemi-biotrophs transition from biotrophy to necrotrophy? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55 3. A new model for S. sclerotiorum pathogenicity? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56 3.1. Plant defense suppression and the role of oxalic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56 3.2. Cell death intricacies between S. sclerotiorum and its host . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 4. Conclusion and prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 * Corresponding author at: Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA. Tel.: +1 979 862 4788. E-mail address: mbdickman@tamu.edu (M.B. Dickman). 1 These authors contributed equally to this work. 1. Introduction Evidence of plant–fungal interactions can be traced back to the Devonian Period, some 450 million years ago [1], long before the appearance of terrestrial vertebrates. Over time, this long period of co-evolution has fostered a diverse combination of pathogenic http://dx.doi.org/10.1016/j.plantsci.2014.12.018 0168-9452/© 2015 Published by Elsevier Ireland Ltd.