The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy

Abstract

Autophagy is a major nutrient recycling mechanism in plants. However, its functional connection with programmed cell death (PCD) is a topic of active debate and remains not well understood. Our previous studies established the plant metacaspase AtMC1 as a positive regulator of pathogen-triggered PCD. Here, we explored the linkage between plant autophagy and AtMC1 function in the context of pathogen-triggered PCD and aging. We observed that autophagy acts as a positive regulator of pathogen-triggered PCD in a parallel pathway to AtMC1. In addition, we unveiled an additional, pro-survival homeostatic function of AtMC1 in aging plants that acts in parallel to a similar pro-survival function of autophagy. This novel pro-survival role of AtMC1 may be functionally related to its prodomain-mediated aggregate localization and potential clearance, in agreement with recent findings using the single budding yeast metacaspase YCA1. We propose a unifying model whereby autophagy and AtMC1 are part of parallel pathways, both positively regulating HR cell death in young plants, when these functions are not masked by the cumulative stresses of aging, and negatively regulating senescence in older plants. An emerging theme in cell death research is that cellular processes thought to be regulated by linear signaling pathways are, in fact, complex. Autophagy, initially considered merely a nutrient recycling mechanism necessary for cellular homeostasis, was recently shown to regulate cell death, mechanistically interacting with components that control apoptosis. Deficient autophagy can result in apoptosis [1][2][3] and autophagy hyper-activation can also lead to programmed cell death (PCD). 4 In addition, the pro-survival function of autophagy is mediated by apoptosis inhibition and apoptosis mediates autophagy, although this cross-regulation is not fully understood. 5In plants, autophagy can also have both pro-survival and pro-death functions. Autophagy-deficient plants exhibit accelerated senescence, 6-8 starvation-induced chlorosis, 6,7,9 hypersensitivity to oxidative stress 10 and endoplasmic reticulum stress.11 Further, autophagy-deficient plants cannot limit the spread of cell death after infection with tissue-destructive microbial infections.12,13 The plant phytohormone salicylic acid (SA) mediates most of these phenotypes.8 Autophagy has an essential, pro-survival role in situations where there is an increasing load of damaged proteins and organelles that need to be eliminated, that is, during aging or stress. Autophagy has an opposing, pro-death role during developmentally regulated cell death 14,15 or during the pathogentriggered hypersensitive response PCD (hereafter, HR) that occurs locally at the site of attempted pathogen attack. 16,17The dual pro-death/pro-survival functions of plant autophagy remain a topic of active debate.Also under scrutiny are possible novel functions of caspases and caspase-like proteins as central regulators of pro-survival processes. Caspases were originally defined as executioners of PCD in an...

Spatial and temporal transcriptome changes occurring during flower opening and senescence of the ephemeral hibiscus flower,Hibiscus rosa-sinensis

“…During hibiscus flower senescence, the nitrogen, phosphorus, potassium, and micro-nutrient content of petals and S-S+S is significantly reduced, supporting a possible role of autophagy in the degradation and remobilization of macromolecules during flower ageing (Trivellini et al , 2011 c ). These data support the previously documented role for autophagy in petal senescence (Yamada et al , 2009; Shibuya et al , 2013), pointing out also its role in senescing S-S+S as a major nutrient recycling mechanism in plants as suggested by Coll et al (2014). Many of the senescence upregulated genes that have been identified from petals and S-S+S tissues encode nucleases and proteases, which are catabolic enzymes involved in the breakdown of nucleic acids and proteins, respectively (Diaz-Mendoza et al , 2014; Sakamoto and Takami, 2014) (Supplementary Table S15).…”

Aspartyl Protease-Mediated Cleavage of BAG6 Is Necessary for Autophagy and Fungal Resistance in Plants

“…Several genes have been shown to modulate cell death and potentially alter immune responses in Arabidopsis, including LOL1 (Epple et al, 2003), LSD1 (Torres et al, 2005), and metacaspases (Coll et al, 2010). Premature senescence and spreading lesions also occur in autophagydeficient plants as a result of accumulation of ubiquitinated proteins and with ER stress (Coll et al, 2014;Munch et al, 2014). Therefore, these plants can be primed for pathogen compatibility (Hackenberg et al, 2013).…”

Retromer Contributes to Immunity-Associated Cell Death in Arabidopsis

“…Using loss-of-function mutants of Arabidopsis thaliana AUTOPHAGY-RELATED (ATG) genes, we provided genetic evidence that HR conditioned by activated TIR-NB-LRR proteins (i.e., RPS4 and RECOGNITION OF PERONOSPORA PARASITICA1) largely depends on autophagy processes (Hofius et al, 2009). Autophagy components also contribute to HR mediated by RPM1, as do other PCD pathways involving metacaspases, cathepsins, and the proteasome (Hofius et al, 2009;Pajerowska-Mukhtar and Dong, 2009;Coll et al, 2010Coll et al, , 2014Hackenberg et al, 2013).…”