Elsevier

Plant Science

Volume 233, April 2015, Pages 53-60
Plant Science

Review
Pathogenic attributes of Sclerotinia sclerotiorum: Switching from a biotrophic to necrotrophic lifestyle

https://doi.org/10.1016/j.plantsci.2014.12.018Get rights and content

Highlights

  • We discuss the current lifestyle designations of plant pathogenic fungi.

  • Host defenses may influence lifestyle transitions in hemi-biotrophs.

  • Sclerotinia sclerotiorum is not a typical necrotroph.

  • We discuss combining fungal lifestyle attributes with damage response curves.

Abstract

Plants and fungi have had many years of friendly and not-so friendly competition for resources and quality 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 consider the contribution of both the fungus and the host to pathogenesis, may provide a more holistic manner to view plant pathogens.

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 interactions. This is evidenced by the impressive number of distinct, but overlapping, morphological and biochemical toolkits developed and utilized by fungi during their association with the host plants. As a consequence of this well-documented arms race, fungi have evolved and adapted complex strategies that tap into and control host pathways by both convergent and divergent evolution. Indeed, common evolutionary branches contain species equipped with a spectrum from very specific to broad host ranges, as well as species with diverse trophic lifestyles. Traditionally, the lifestyles of plant pathogenic fungi have been divided into distinct groups predicated on nutrient acquisition and the viability of host tissue. Biotrophs extract nutrients from living cells; via specialized feeding structures (i.e. haustoria), and generally lack toxin production and secrete few cell wall degrading enzymes (CWDEs). Necrotrophs feed off killed cells, and produce several toxins and CWDEs. Lastly, hemi-biotrophs exhibit characteristics of both biotrophs and necrotrophs, initially invading living cells prior to a transition to a necrotrophic lifestyle in which nutrients are obtained from host cells that they kill.

Necrotrophic fungi kill host tissue via the secretion of a battery of toxins and degradative enzymes often in advance of fungal growth and colonization of the host, in the field as well as post-harvest [2], [3], [4], [5], [6]. These degradative enzymes penetrate the host and subsequently degrade cell wall components that then serve as carbon sources. This lifestyle has bestowed upon this group of pathogens the reputation or perception as brutish and unsophisticated in their “dining habits” as illustrated by impressively broad host ranges associated with several members of this group. Indeed, the recent genomic sequence analyses of two prototypical fungal necrotrophs, Sclerotinia sclerotiorum and Botrytis cinerea [7] revealed over 100 potential carbohydrate-active enzyme (CAZyme) encoding genes. In contrast, the fungal biotroph Blumeria graminis possesses only 10, a significantly smaller hydrolytic enzyme arsenal, consistent with its obligate biotrophic lifestyle [8]. However, the CAZyme content of both B. cinerea and S. sclerotiorum is equivalent or even lower than presumably more adapted fungal pathogens such as Magnaporthe oryzae and Gibberella zeae, both well studied hemi-biotrophic fungal pathogens. Further, the saprotrophic ascomycetes, Aspergillus nidulans and Aspergillus niger, possess approximately 100 genes encoding predicted enzymes capable of digesting plant cell wall polymers. Though gene expression within this repertoire is likely to vary among fungal organisms, as well as being fine-tuned to particular host or substrate. It is however clear that, with the exception of obligate biotrophs, there is no clear correlation between cell wall degrading enzyme capacity and trophic lifestyle [9]. While at first glance these observations might be unexpected, these enzymes are likely important when the fungus is living under saprophytic conditions, which constitute in some cases a significant portion of a pathogen's life, and therefore may be primarily used to break down plant debris. These categories, while operationally correct, are not black and white, and trophic designations may need to be revisited as more experimental evidence becomes available.

Effectors, small proteins secreted by various phytopathogens, often modulate host responses to the pathogen. Studies designed to elucidate effector targets and function is an active area of current research in plant–microbe interactions [10], [11]. Their role in virulence in several biotrophic and hemi-biotrophic interactions is well documented, while their functions in other pathosystems await characterization. Effectors can also contribute to virulence by suppressing plant basal defense responses that would otherwise be triggered in response to conserved microbial features, the pathogen associated molecular patterns (PAMPs). One example of a fungal PAMP is chitin, a constituent of fungal cell walls. Thus, due to (or following) PAMP-triggered immune responses, the presence of fungal effectors can be key determinants in the successful (vis a vis the pathogen) outcome in a fungal–host interaction. Effectors can be directly or indirectly recognized by resistance (R) proteins in the host, and activate a strong defense response, the effector-triggered immunity that often culminates in programmed cell death (PCD) of plant cells. Excluding host selective toxins [12], [13], the importance or deployment of necrotrophic effectors in the infection process is not clear. This may partly be due to the fact that R-mediated resistance against necrotrophs has not been found, and because necrotrophs are thought to possess considerable direct weaponry (secondary metabolites, CWDEs), presumably circumventing the need for such effectors. Nevertheless, sequence data from both S. sclerotiorum and B. cinerea revealed an abundance of small secreted plant inducible proteins that could serve as effectors. In S. sclerotiorum alone, there are 603 genes encoding secreted proteins, of which, 193 are smaller than 150 amino acids [7]. While these correlations await functional proof, it is tempting to speculate that bona fide effectors have a role in this pathosystem as multiple candidates have been identified [14]. In the case of one of these S. sclerotiorum effectors, as discussed later, there are clear indications for a role in pathogenesis [15]. The importance/involvement of effectors in necrotroph–plant interactions awaits further bioinformatic analysis coupled with systematic functional examination. Overall, at the sequence level, unique necrotrophic pathogenicity determinants have proven difficult to single out. Genome sequences of necrotrophs were expected to inform us of the outcome of their evolution, but so far have failed to reveal necrotroph-specific components.

S. sclerotiorum is a cosmopolitan necrotrophic fungal pathogen with a broad host range (>400 plant species). A key factor governing the pathogenic success of this fungus is the synthesis and secretion of oxalic acid, and S. sclerotiorum mutants defective in oxalate production cause limited lesions [16], [17], [18]. Oxalic acid contributes to pathogenesis in a significant number of ways that augment fungal colonization of host plants, such as the acidification of host tissues and sequestration of calcium from host cell walls, to facilitate the action of cell wall degrading enzymes. In the past few years several additional functions associated with oxalate have been uncovered, including the induction of a PCD response in plant tissue that is required for disease development, adding to the continuing multi-functional nature of this “simple” organic acid [19], [20]. Studies with oxalate deficient mutants have shown that this molecule is a key suppressor of plant defenses; thus allowing the fungus to evade recognition [21]. In the absence of oxalate, the host plant is able to recognize the invading pathogen, and mount a defense response that includes a pronounced oxidative burst and callose deposition. Though models describing recognition and response to pathogens have mostly focused on plant interactions with biotrophs and hemi-biotrophs, it is evident that S. sclerotiorum is able to alter the plant recognition process at least in part, via the secretion of oxalate. The regulation of redox homeostasis plays a key role in this process; oxalate initially dampens the host oxidative response (as part of a potential biotrophic interaction) before triggering reactive oxygen species (ROS) at the later stages of infection, culminating in PCD (the advanced necrotrophic phase of the interaction) and disease [21]. S. sclerotiorum, via oxalate, has also been shown to induce apoptotic-like cell death in the host [20]. However, in its absence, the coordinated defense response against this pathogen involves autophagic cell death [15], which has been suggested to be involved in the regulation of the plant hypersensitive response [22]. Therefore, during S. sclerotiorum interactions with the host plant, the occurrence of PCD can confer both resistant and susceptible outcomes. The multi-functionality of oxalate, including the suppression of defenses and autophagy, can allow the fungus valuable time for establishment of infection. This has been traditionally regarded as a feature associated with hemi-biotrophic growth.

In general, biotrophic fungi as well as several hemi-biotrophs have been shown to hijack and redirect host pathways as a major means for pathogenic success. Part of the biotrophic process involves obtaining nutrients from living cells while suppressing host immune responses. A universal defense response against these pathogens culminates in PCD. The Hypersensitive cell death was generally thought to be conducive for necrotrophic infection [23]. However, recent studies with several necrotrophs suggest that the infection process may be more subtle than originally conceived, and that certain necrotrophs do not simply thrive on mere killing [21]. Moreover, our recent work indicates these pathogens do not kill the cell directly but instead commandeer PCD pathways, for their own benefit [15]. Therefore, killing per se is neither beneficial nor detrimental, but is rather context dependent. This has been clearly shown in the S. sclerotiorum system, where the manner by which cell death occurs is key to the outcome [15]. Although the mechanistic details allowing these pathogens to control host metabolic pathways are not entirely known, emerging evidence will be discussed from the S. sclerotiorum pathosystem. In part, this review focuses on this pathosystem due to the current advances describing the association of S. sclerotiorum and its host plants, and highlights important issues associated with the perception of necrotrophic pathogenesis. Thus, based on this recent progress, we propose that the pathogenic development of this prototypical necrotroph is more aligned with an adaptable lifestyle.

Section snippets

Why do hemi-biotrophs transition from biotrophy to necrotrophy?

Molecular and physiological factors governing the transition from biotrophy to necrotrophy in hemi-biotrophic fungal pathogens have been largely elusive. Extended periods of biotrophic colonization are required for several hemi-biotrophs to establish infection. For others, hours suffice for successful infection and the switch to necrotrophy rapidly occurs. One question is how long does a biotrophic phase need to last? One possible answer is that biotrophy is needed long enough to thwart host

Plant defense suppression and the role of oxalic acid

One of the characteristics of biotrophic and early stage hemi-biotrophic fungal pathogens is their ability to suppress host defenses and avoid recognition. When this suppression is compromised, a strong plant defense response effectively arrests infection. S. sclerotiorum is an ascomycete with a reported necrotrophic lifestyle that infects virtually all dicotyledonous plants. As mentioned above, S. sclerotiorum secretes oxalate, which is central to its pathogenic success. The role of oxalate in

Conclusion and prospects

As described in this review, several host pathogen interactions have defined biotrophic and necrotrophic lifestyles. However, as the molecular, genetic and mechanistic analyses of pathogenic fungi progress, we are witnessing potential deviations from the somewhat rigid lifestyle categorization of certain fungal pathogens. S. sclerotiorum, has been the example focus of this review. While describing a fungal lifestyle is based on the available data at a given time, perhaps the re-evaluation of

Acknowledgments

We thank Drs. Paul de Figueiredo, Brett Williams, and Damon L. Smith for their stimulating discussions. We thank Dr. Mingde Wu for his assistance with the figures. Funding for this work was in part provided by National Science Foundation (MCB-092391) to MBD, Binational Agricultural Research and Development Fund (US-4041-07C) to MBD and OY, and Wisconsin Soybean Marketing Board (MSN172403) to MK.

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    These authors contributed equally to this work.

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