Functions and Regulation of Programmed Cell Death in Plant Development

Daneva, Anna; Gao, Zhen; Durme, Matthias Van; Nowack, Moritz K.

doi:10.1146/annurev-cellbio-111315-124915

Cited by 202 publications

(170 citation statements)

References 177 publications

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“…Tonoplast rupture is a plant‐specific feature of vacuolar PCD (van Doorn et al ., ) and we showed it occurring here during ERSID induced by protein misfolding, as shown also for ERSID induced by the mutualistic fungi Piriformospora indica in root cells (Qiang et al ., ). Tonoplast rupture is considered a point of no return during plant PCD as degrading enzymes as expected to be released from the vacuole into the cytoplasm and degrade cellular components (Daneva et al ., ). Interestingly, cathepsin B downregulation reduced ERSID, but did not block tonoplast rupture as VPE did.…”

Section: Discussionmentioning

confidence: 97%

Two proteases with caspase‐3‐like activity, cathepsin B and proteasome, antagonistically control ER‐stress‐induced programmed cell death in Arabidopsis

Cai

et al. 2017

New Phytologist

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Summary Programmed cell death (PCD) induced by endoplasmic reticulum (ER) stress is implicated in various plant physiological processes, yet its mechanism is still elusive. An activation of caspase‐3‐like enzymatic activity was clearly demonstrated but the role of the two known plant proteases with caspase‐3‐like activity, cathepsin B and proteasome subunit PBA1, remains to be established.Both genetic downregulation and chemical inhibition were used to investigate the function of cathepsin B and PBA1 in ER‐stress‐induced PCD (ERSID). Transcript level and activity labelling of cathepsin B were used to assess activation. To study tonoplast rupture, a plant PCD feature, both confocal and electronic microscopies were used.Cathepsin B downregulation reduced reactive oxygen species (ROS) accumulation and ERSID without affecting the induction of the unfolded protein response (UPR), but downregulation of PBA1 increased UPR and ERSID. Tonoplast rupture was not altered in the cathepsin B mutant and cathepsin B activation was independent of vacuolar processing enzyme (VPE). VPE activity was independent of cathepsin B. ERSID is regulated positively by cathepsin B and negatively by PBA1, revealing a complex picture behind caspase‐3‐like activity in plants. Cathepsin B may execute its function after tonoplast rupture and works in parallel with VPE.

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Section: Discussionmentioning

confidence: 97%

Two proteases with caspase‐3‐like activity, cathepsin B and proteasome, antagonistically control ER‐stress‐induced programmed cell death in Arabidopsis

Cai

et al. 2017

New Phytologist

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“…The cytc mutants under study also have normal ascorbic acid levels (Welchen et al, 2012), suggesting that deficiencies in ascorbic acid metabolism are not responsible for the observed effects of CYTc deficiency. If any, the role of CYTc in PCD in plants, unlike the situation in animals, is far from being understood (Daneva et al, 2016). Although an effect of defective PCD on growth and GA homeostasis in cytc mutants cannot be completely ruled out, current evidence indicates that developmental PCD is required for the differentiation of specific cell types, rather than for generalized plant growth (Daneva et al, 2016).…”

Section: Inhibition Of Mitochondrial Energy Metabolism Mimics the Effmentioning

confidence: 99%

“…If any, the role of CYTc in PCD in plants, unlike the situation in animals, is far from being understood (Daneva et al, 2016). Although an effect of defective PCD on growth and GA homeostasis in cytc mutants cannot be completely ruled out, current evidence indicates that developmental PCD is required for the differentiation of specific cell types, rather than for generalized plant growth (Daneva et al, 2016). Thus, in view of our results and the existing literature we favor the hypothesis that altered GA homeostasis and defective growth in cytc mutants are due to the role of CYTc in energy metabolism.…”

Section: Inhibition Of Mitochondrial Energy Metabolism Mimics the Effmentioning

confidence: 99%

Interplay between cytochrome c and gibberellins during Arabidopsis vegetative development

et al. 2018

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We studied the effect of reducing the levels of the mitochondrial electron carrier cytochrome c (CYTc) in Arabidopsis thaliana. Plants with CYTc deficiency have delayed growth and development, and reach flowering several days later than the wild-type but with the same number of leaves. CYTc-deficient plants accumulate starch and glucose during the day, and contain lower levels of active gibberellins (GA) and higher levels of DELLA proteins, involved in GA signaling. GA treatment abolishes the developmental delay and reduces glucose accumulation in CYTc-deficient plants, which also show a lower raise in ATP levels in response to glucose. Treatment of wild-type plants with inhibitors of mitochondrial energy production limits plant growth and increases the levels of DELLA proteins, thus mimicking the effects of CYTc deficiency. In addition, an increase in the amount of CYTc decreases DELLA protein levels and expedites growth, and this depends on active GA synthesis. We conclude that CYTc levels impinge on the activity of the GA pathway, most likely through changes in mitochondrial energy production. In this way, hormone-dependent growth would be coupled to the activity of components of the mitochondrial respiratory chain.

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“…Despite the functional conservation of PCD across a broad evolutionary diversity, it is also crucial for plant reproduction in multiple flower tissues and cells (Daneva et al, 2016). Moreover, autophagic cell death, which is regarded as one of the major PCD types, has been well studied in animals, including in C. elegans and D. melanogaster (Martin et al, 2007;Samara et al, 2007;Mariño et al, 2014).…”

Section: Possible Interplay Between Autophagy and Programmed Cell Deamentioning

confidence: 99%

Boosting autophagy in sexual reproduction: a plant perspective

Mei

et al. 2020

New Phytologist

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Summary The key process of sexual reproduction is the successful fusion of the sperm and egg cell. Distinct from dynamic and flagellated animal sperm cells, higher flowering plant sperm cells are immotile. Therefore, plants have evolved a novel reproductive system to achieve fertilization and generate progenies. Plant sexual reproduction consists of multiple steps, mainly including gametophyte development, pollen–pistil recognition, pollen germination, double fertilization and postfertilization. During reproduction, active production, consumption and recycling of cellular components and energy are critically required to achieve fertilization. However, the underlying machinery of cellular degradation and turnover remains largely unexplored. Autophagy, the major catabolic pathway in eukaryotic cells, participates in regulating multiple aspects of plant activities, including abiotic and biotic stress resistance, pathogen response, senescence, nutrient remobilization and plant development. Nevertheless, a key unanswered question is how autophagy regulates plant fertilization and reproduction. Here, we focus on comparing and contrasting autophagy in several key reproductive processes of plant and animal systems to feature important distinctions and highlight future research directions of autophagy in angiosperm reproduction. We further discuss the potential crosstalk between autophagy and programmed cell death, which are often considered as two disconnected events in plant sexual reproduction.

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Functions and Regulation of Programmed Cell Death in Plant Development

Cited by 202 publications

References 177 publications

Two proteases with caspase‐3‐like activity, cathepsin B and proteasome, antagonistically control ER‐stress‐induced programmed cell death in Arabidopsis

Two proteases with caspase‐3‐like activity, cathepsin B and proteasome, antagonistically control ER‐stress‐induced programmed cell death in Arabidopsis

Interplay between cytochrome c and gibberellins during Arabidopsis vegetative development

Boosting autophagy in sexual reproduction: a plant perspective

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