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Metacaspases in Plants and Fungi: Comparison
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Please note this is a comparison between Version 1 by Rachel E Kalicharan and Version 2 by Amina Yu.

Plant pathogens are responsible for devastating agricultural losses across a wide array of crops, exacerbating the burden of global food insecurity. Successful plant pathogens must bypass plant defenses while plants must employ a vast range of controlled defense mechanisms to subvert potential pathogenicity. This complex interaction entails utilizing a variety of mechanisms, such as pathogen effector proteins and host resistance genes. Intriguingly, a common denominator observed in these plant-pathogen interactions is the implementation and regulation of cellular death. Plant immune responses rely on precise and regulated cell death to impede pathogen invasion while ensuring the protection of the surrounding host cells. Conversely, cell death is an important aspect in the maintenance of pathogen fitness, as it enables the pathogen to effectively cause disease and circumvent defense strategies executed by the plant host.

  • metacaspases
  • programmed cell death
  • plant immunity
  • pathogenicity
  • fungal pathogens

1. What Are Plant Metacaspases Cleaving?

While an overexpression of metacaspases and regulation of programmed cell death (PCD) can be seen in various plant organisms after pathogen infection, less is known about the substrates targeted by plant metacaspases. During PTI, the plant is also able to sense internal host molecules known as damage-associated molecular patterns (DAMPs) to trigger defense responses [1]. Plant elicitor peptides (Peps) are DAMPs that can be released during pathogen invasion [2]. Peps themselves are produced via the cleavage of their precursor proteins, PROPEPs, which is a component of the plant innate immune response [3]. Previously, it was unknown what exactly regulated the production of Peps during PTI. An in vitro study on the metacaspase AtMC4 from A. thaliana showed AtMC4 to be important for Pep1 maturation from PROPEP1, and this interaction promoted defense responses in the plant following mechanical damage to plant tissue [4]. A subsequent study done with A. thaliana protoplasts confirmed the cleavage of PROPEP1 by AtMC4 [5]. This in-depth study also reported that the bacterial elicitor flg22 increased PROPEP1 expression and promoted AtMC4-mediated cleavage of PROPEP1, most likely due to flg22-induced Ca2+ accumulation which further promoted AtMC4 activity [5]. Together, these studies demonstrate the interconnection between plant immunity mechanisms and metacaspase regulation. AtMC4 is able to provide a direct pathway for plant defense responses following both mechanical damage and pathogen invasion through controlling the rate of Pep1 production. Furthermore, the upregulation of AtMC4 in response to mechanical damage poses the question if the level of metacaspase expression bears a direct relationship to the degree of damage sustained by the plant host. More specifically, such an investigation can reveal if there is cross talk between the PAMP and DAMP pathways, or if certain proteins are strictly confined to specific pathways/means of compromise.
Most recently, an A. thaliana metacaspase was found to be involved in helping trigger PTI [6]. The plasma membrane-anchored receptor-like cytoplasmic kinase PBS1-LIKE 19 (PBL19) normally is tethered to the plasma membrane. Following chitin recognition by the receptor LYSM-CONTAINING RECEPTOR-LIKE KINASE 5 (LYK5) and co-receptor CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1), PBL19 is translocated to the nucleus via its nuclear localization signal (NLS). Through the cleavage of the NLS of PBL19 by AtMC4, the metacaspase-cleaved PBL19 alters its localization from the nucleus to the cytoplasm [6]. This change in localization allows for the metacaspase-cleaved PBL19 to phosphorylate a known regulator of PCD, ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), and in turn, amplify plant defense signals [6]. This finding expands on the functionality of plant metacaspases that are involved in enhancing plant immunity against plant pathogens through altering the localization of immune system regulators. EDS1 has also previously been linked to promoting ETI in A. thaliana [7]. Further characterizing the overlap of EDS1 in immunity may help bridge the gap between the two major immune responses in plants.
Additionally, recent research has also shown links between metacaspase activity and ETI. In grapevine, two metacaspases, VrMC2 and VrMC5 were found to be upregulated following infection with the pathogen Plasmopara viticola [8]. Interestingly, in grapevine lines overexpressing either VrMC2 or VrMC5 showed HR induction with the bacterial elicitor, harpin [8]. These cell death events were shown to be mediated by ROS bursts in the apoplast facilitated by a plasma membrane-located NADPH oxidase [8]. These results demonstrate potential downstream pathways that could be involved in metacaspase activation to promote immune related responses.
Furthermore, the A. thaliana metacaspases, AtMC1 and AtMC2, had previously demonstrated a role in regulating PCD following Pseudomonas syringae infection through either positively or negatively controlling pathogen-triggered HR via NLR interaction, respectively [9]. It is known that activation of NLR is directly associated with the upregulation of defense-related genes [10]. Therefore, metacaspase association with NLR mechanisms seems to be crucial for apt PCD in response to pathogens. This was validated when research conducted on maize (Zea mays) metacaspases provided further insight into the way in which metacaspase activity mediates HR through the modulation of a maize R gene coding for an NLR protein, Rp1-D21 [11]. It was shown that two type I metacaspases, ZmMC1 and ZmMC2, were involved in suppressing Rp1-D21-mediated HR in N. benthamiana, likely through an interaction with the coiled-coil domain of Rp1-D21 [11]. When Rp1-D21 was infiltrated via Agrobacterium-mediated transient expression without ZmMC1 or ZmMC2, N. benthamiana leaves showed HR symptoms, but the symptoms were reduced following the co-expression of ZmMC1 or ZmMC2 and Rp1-D21 [11]. Additional studies showed ZmMC1 and ZmMC2 altered Rp1-D21 subcellular localization from a uniform distribution in the nucleocytoplasm to a more punctate co-localization with ZmMC1 and ZmMC2 [11]. It was found through co-immunoprecipitation and yeast-two-hybrid assays that the physical association of Rp1-D21 N-terminal coiled-coil (CCD21) with ZmMC1 and ZmMC2 promoted the regulation of HR. In all, ZmMC1 and ZmMC2 have been shown to act similar to AtMC2 in A. thaliana given their functions in negatively regulating plant immune responses [9][11]. While maize seems to contain 11 different metacaspases, only ZmMC1 and ZmMC2 were shown to have this negative regulation to HR through their interaction with Rp1-D21. Other metacaspases that did not interact with Rp1-D21, such as ZmMC9, did not colocalize with Rp1-D21 or negatively affect cell death symptoms. While there was no evidence of cleavage or lytic activity from ZmMC1 or ZmMC2, the researchers suggest ZmMC1 or ZmMC2 work instead to aggregate Rp1-D21 inside of the cell, preventing it from localizing in a different compartment that may trigger HR.
Surprisingly, the autophagy marker, Atg8a, colocalizes in the punctate localizations along with ZmMC1 and ZmMC2 suggesting that both metacaspases are localized in autophagosomes [11]. The researchers thus speculate that Rp1-D21 is translocated to autophagosomes through interactions with ZmMC1 and ZmMC2, and Rp1-D21 is potentially taken to the vacuole for degradation to inhibit HR [11]. This finding is interesting given that previous investigations showed AtMC1-mediated PCD to act independently of autophagy pathways, suggesting that there are parallel pathways involved in mediating pathogen-triggered HR in plants [12]. Further studies need to be conducted in order to better understand if the suppression of HR is done through ZmMC1 and ZmMC2 regulating the localization of Rp1-D21 and acting in association with the autophagy pathway. Moreover, the N. benthamiana infiltrations of ZmMC1, ZmMC2, and Rp1-D21 were conducted without any calcium supplementation. Either Ca2+ levels within the plant were enough to promote activation of ZmMC1 and ZmMC2, or aggregation of Rp1-D21 did not require metacaspase activation and would point to additional functionalities of metacaspases that are calcium-independent. The presence of multiple pathways to tightly regulate metacaspase activity and PCD demonstrates their critical nature to host viability and homeostasis, as well as host adaptability and versatility to various situations that would require metacaspase-mediated PCD.

2. Plant Development, Stress Responses, and Cell Death

The roles of plant metacaspases expand beyond plant immune responses. While not in the scope of therein, is review, we will lightly highlight metacaspase functionality in plant development and stress responses will be lightly highlighted. For instance, numerous metacaspases identified in grapes showed increased expression during ovule development [13]. Two metacaspases from Populus trees have also reportedly been involved in cell death of xylem elements [14]. A study done on the metacaspase mcII-Pa from Norway spruce (Picea abies) demonstrated that during plant embryogenesis, mcII-Pa translocated from the cytoplasm to the nucleus to promote vacuolar cell death through DNA fragmentation [15][16]. A follow up study conducted on mcII-Pa demonstrated that in the absence of mcII-Pa or autophagy activity, previously expected vacuolar cell death activity shifted to necrotic cell death [17]. It seems that in P. abies, mcII-Pa is essential to maintain PCD through vacuolar cell death activity and, in its absence, PCD mechanisms switch to necrosis. Further questions arise on the specificity that metacaspases may have to certain forms of plant PCD and how their absence or overexpression may impact plant viability, particularly during cellular developmental stages, under certain stress conditions, or during pathogen attacks.
The A. thaliana metacaspase, AtMC8, was reported to exhibit sensitivity to H2O2 and UVC stress; exposure of these stressors when overexpressing AtMC8 resulted in increased levels of PCD [18]. AtMC4 was also shown to be associated with increased sensitivity to a PCD inducer and oxidative stress inducers [19]. The characterization of metacaspases in rice, tomato, and rubber tree showed changes in metacaspase expression levels during increased salt or drought conditions [20][21][22]. This could indicate that metacaspases are one of the primary modulators of controlling PCD as a means to regulate damage done from external stimuli. A recent transcriptome analysis identified Sedum alfredii Metacaspase-1-like (AMC1) protein to be sensitive to heavy metal compounds [23]. Following indium treatment on wheat seedlings, indium-toxicity promoted wheat root cell death through the upregulation of metacaspases TaMCA1 and TaMCA4 [24]. Through a variety of environmental cues, plant metacaspases appear to be involved in a variety of stress responses that aim to protect the plant from undesirable external conditions. How a variety of metacaspases can be triggered through several different stressors remains to be understood. Further dissecting the interplay between metacaspase activated PCD and autophagy may bring additional networks to light that mediate metacaspase activity from stress responses.

3. The Basis for Fungal Metacaspases

The first metacaspase was found in the genome of Saccharomyces cerevisiae, which encodes a singular metacaspase known as Yca1 [25][26]. Like caspases, Yca1 has also been found to be involved in regulating cell death and oxidized proteins in the cell during stress conditions [27]. These findings illuminated a key player involved in the regulation of cell death in fungi. Especially of importance is the N-terminal prodomain of Yca1, which was shown to be needed for the clearance of insoluble aggregates [28]. Recent work has also shown an association between Yca1 and the ubiquitin-proteasome system (UPS) [29]. It was determined that the interaction between an E3 ligase (Rsp5) and Yca1 impacted the role of Yca1 in regulating both cellular vacuolar response and the insoluble aggregate levels in the cell [29]. Ubiquitination of Yca1 at K355 and phosphorylation at S346 promoted the interaction with Rsp5 [29]. Moreover, it was reported that Yca1 cleaved a ubiquitin precursor protein, Rps31, to promote the release of ubiquitin in the cell, in essence functioning as a deubiquitinating enzyme, aiding in maintaining proper ubiquitin concentrations that positively influences the clearance of protein aggregation [29]. Here,This itstudy is the first to establish how Yca1 can influence free ubiquitin in the cell to promote its association with Rsp5 in order to maintain the proteosome in the cell through regulating autophagy and protein aggregation. The interconnection between cellular processes and metacaspases demonstrates the adaptable nature of these proteins and gives insight into how some metacaspases can be responsible for their own activation. Studies in filamentous fungi are necessary to confirm if these interactions extend beyond single cell fungi, which could point to additional associations between metacaspase regulation of the UPS and autophagy pathways to promote adequate proteasome levels in the cell.

3.1. Fungal Metacaspase Involvement in Pathogenicity

Though the identification of metacaspases in plant pathogens are scarce, recent studies characterizing novel metacaspases in Usilago maydis and Magnaporthe oryzae depict metacaspases as multifaceted proteins involved in pathogen fitness and promoting disease in fungal plant pathogens following Ca2+ activation [30][31]. U. maydis is a biotrophic fungus responsible for smut disease in maize. The only metacaspase in U. maydis, Mca1, has been found to have a role in aiding vegetative growth, executing PCD, promoting the clearance of insoluble aggregates during stress conditions, as well as maintaining proper pathogenicity in maize [30]. The two metacaspases found in the hemibiotrophic fungus M. oryzae, MoMca1 and MoMca2, depict similar roles for maintaining proper fitness of the fungus to promote disease [31]. It was found that calcium activated MoMca1 and MoMca2 promoted the clearance of insoluble aggregates and were needed for full pathogenicity in rice [31]. Future studies are needed to explore the ways in which these metacaspases maintain the M. oryzae proteosome. This could point to a potential association between M. oryzae metacaspases and the UPS as was shown with Yca1, which would further explain how M. oryzae is able to promote the clearance of insoluble aggregates. While this study did not show MoMca1 and MoMca2 to be involved in PCD, it did suggest a potential role in stress response as the double metacaspase knockout strain showed increased radial growth on plates following stress tests [31]. The increased radial growth in the absence of MoMca1 and MoMca2 could suggest these metacaspases act as negative regulators of cell death, or perhaps their functionality is independent of PCD. These observations, in conjunction with the diminished stress response, indicate these proteins wield functional duality in vegetative growth and pathogenicity. Furthermore, the localization of MoMca1 and MoMca2 may give potential clues as to additional functions of these metacaspases to see if they are involved in important fungal differentiation stages needed for pathogenicity as was suggested in the delayed development of M. oryzae in the absence of both metacaspases. This delayed development could signify issues with autophagic cell death which is needed for proper growth and infection [32]. Deeper examination may uncover additional relationships between filamentous fungi metacaspases and autophagy in promoting pathogen development and, in effect, pathogenicity. As plant metacaspases work towards strengthening plant immunity and stress responses, plant pathogen metacaspases promote cell fitness to cause disease. The branching of these roles in different organisms demonstrates the complexity of metacaspase proteins especially as they relate to immunity and disease.

3.2. Cell Death Roles of Fungal Metacaspases

Cell death in fungus, much like that of plants, differs from normal animal cell death due to its cell wall and lack of caspase proteins. Characteristics of fungal cell death include DNA fragmentation, cellular shrinkage, increased ROS production, and upregulation of metacaspase activity [33]. Metacaspase activity has been documented in fungi as it relates to ageing and stress responses. For instance, in Podospora anserina, two metacaspases, PaMCA1 and PaMCA2, were shown to be upregulated in older cultures, suggesting their involvement during senescence [34]. Additionally, PaMCA1 expression was increased when cultures were treated with H2O2 [34]. These observations substantiate the multifunctional capacity of fungal metacaspases, delineated in their ability to operate in development, as well as in stimuli and stress responses. Moreover, the role of metacaspases in fungi can be paralleled to that of plant metacaspases, verifying that conserved functions of the protein are not necessarily restricted to a single kingdom.
In non-pathogenic fungi, poly ADP-ribose polymerases (PARPs) have been identified to be targeted by two metacaspases in P. anserina [35]. A PARP-like protein was also shown to be targeted and degraded during sporulation of Aspergillus nidulans [36]. PARPs have been identified as mediating DNA repair in the cell that has been damaged due to stresses [37]. This is similar to mechanisms seen with animal cell caspases, cleaving PARPs and promoting cell death [38]. A similar substrate was identified for both S. cerevisiae and the protozoan parasite Trypanosoma brucei [39]. Both S. cerevisiae and T. brucei were shown to cleave in vitro the DNA-damage inducible protein 1 (Ddi1), another evolutionary conserved eukaryotic shuttle protein that interacts with the UPS. In yeast, the cleavage of Ddi1 by Yca1 only occurred after increasing Ca2+ concentrations in the cell [39]. Expanding on this interaction may yield more information on the ways in which metacaspases interact with the UPS to promote proteolytic events to maintain the proteosome in the cell. Additional characterization of metacaspase substrates in other fungal species will further illustrate the distinct cell death mechanisms employed by fungi during stress conditions.

4. Future Perspectives

It is becoming increasingly evident the vital role metacaspases hold in plant-pathogen interactions. On the plant side, metacaspases can be critical in the prevention of pathogenicity, while on the fungal side, they can promote evasion of host defenses. Plant metacaspases have been more extensively researched, giving insight into their wide range of functions in development, immunity activation, stress response, and PCD regulation. Follow-up studies on these discoveries could reveal interactions of metacaspases with other pathways or compounds involved in regulating these functions. Similarly, while Yca1 has led to many identifications of metacaspase homologs in higher fungal species, it will be interesting to see if future studies find additional associations between plant pathogen metacaspases and developmental stages, ageing, or interactions with the UPS. Examining the evolutionary trajectory of fungal metacaspases can further illuminate additional functionalities or even functional redundancies. In a relationship that is constantly described as an arms race, it will be fascinating to continue dissecting the roles of metacaspases within plant-pathogen interactions. For instance, do pathogen metacaspases counteract plant metacaspase activity? Does enhancing metacaspase activity in plants or inhibiting fungal metacaspases prevent disease proliferation? Through an agricultural lens, including and considering the influence of metacaspases on both ends of the disease can lead to more robust and concentrated mitigation strategies. Approaches that focus on the influence of metacaspases in disease incidence and prevention can provide a molecular basis of understanding virulence and defense mechanisms, ultimately increasing the production rate of globally relevant food sources. Metacaspases are undoubtedly a critical factor in plant-pathogen interactions, and going forward, diving deeper into the incidence and evasion of plant disease must also mean exploring the roles and involvement of metacaspases.

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