A Bipartite Molecular Module Controls Cell Death Activation in the Basal Cell Lineage of Plant Embryos

Zhao, Peng; Zhou, Xuemei; Zhang, Liyao; Wang, Wei; Ma, Ligang; Yang, Libo; Peng, Xiongbo; Bozhkov, Peter V.; Sun, Mingwei

doi:10.1371/journal.pbio.1001655

Cited by 73 publications

(83 citation statements)

References 39 publications

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“…A similar posttranslational protease regulation by cystatins has been hypothesized for germinating barley seeds (Martinez et al, 2009). The tight regulation of proteases by cystatins has also been demonstrated in tobacco embryos (Zhao et al, 2013), illustrating the need to monitor these protease activities individually to unravel their functions.…”

Section: Discussionmentioning

confidence: 55%

“…Proteases from both families are produced as inactive precursors that require processing in order to remove inhibitory propeptides (Kuroyanagi et al, 2002;Gu et al, 2012). Furthermore, both classes of proteases are tightly regulated by endogenous inhibitors such as cystatins and serpins (Lampl et al, 2013;Zhao et al, 2013). Because of their posttranslational regulations, it is impractical to predict activities of PLCPs and VPEs from transcript abundance.…”

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confidence: 99%

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Subfamily-Specific Fluorescent Probes for Cysteine Proteases Display Dynamic Protease Activities during Seed Germination

Chandrasekar

Oeljeklaus

et al. 2015

Plant Physiology

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Cysteine proteases are an important class of enzymes implicated in both developmental and defense-related programmed cell death and other biological processes in plants. Because there are dozens of cysteine proteases that are posttranslationally regulated by processing, environmental conditions, and inhibitors, new methodologies are required to study these pivotal enzymes individually. Here, we introduce fluorescence activity-based probes that specifically target three distinct cysteine protease subfamilies: aleurain-like proteases, cathepsin B-like proteases, and vacuolar processing enzymes. We applied protease activity profiling with these new probes on Arabidopsis (Arabidopsis thaliana) protease knockout lines and agroinfiltrated leaves to identify the probe targets and on other plant species to demonstrate their broad applicability. These probes revealed that most commercially available protease inhibitors target unexpected proteases in plants. When applied on germinating seeds, these probes reveal dynamic activities of aleurain-like proteases, cathepsin B-like proteases, and vacuolar processing enzymes, coinciding with the remobilization of seed storage proteins.

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Section: Discussionmentioning

confidence: 55%

mentioning

confidence: 99%

Subfamily-Specific Fluorescent Probes for Cysteine Proteases Display Dynamic Protease Activities during Seed Germination

Chandrasekar

Oeljeklaus

et al. 2015

Plant Physiology

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“…The suspensors of 8-and 32-celled embryos developed into second embryos, whereas those at or beyond the heart stage did not. This may be because suspensors at this stage are already entering the process of programmed cell death (35) and are unable to reprogram their fate, although the cells are still living.…”

Section: Discussionmentioning

confidence: 99%

Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis

Liu

Zhao

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The suspensor is a temporary supporting structure of proembryos. It has been proposed that suspensor cells also possess embryogenic potential, which is suppressed by the embryo as an effect of the embryo–suspensor interaction. However, data to support this hypothesis are not yet available. In this report, using an in vivo living cell laser ablation technique, we show that Arabidopsis suspensor cells can develop into embryos after removing the embryo proper. The embryo proper plays a critical role in maintaining suspensor cell identity. However, this depends on the developmental stage; after the globular embryo stage, the suspensors no longer possess the potential to develop into embryos. We also reveal that hypophysis formation may be essential for embryo differentiation. Furthermore, we show that, after removing the embryo, auxin gradually accumulates in the top suspensor cell where cell division occurs to produce an embryo. Auxin redistribution likely reprograms the fate of the suspensor cell and triggers embryogenesis in suspensor cells. Thus, we provide direct evidence that the embryo suppresses the embryogenic potential of suspensor cells.

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“…Although cystatin family genes have been identified in some plant species, only a few cystatins in plants have been well characterized, which show their function in programmed cell death (Solomon et al 1999;Zhao et al 2013), seed germination (Hwang et al 2009), plant defense against pathogens (Belenghi et al 2003;Gutierrez-Campos et al 1999), response to insect attack (Goulet et al 2008;Konrad et al 2008) and abiotic environmental stresses (Hwang et al 2010). These works reveal that plant cystatins are crucial to several essential processes in plant development as described above, especially in the process of sexual plant reproduction and abiotic/biotic stresses, suggesting that cystatins are critical not only for plant vegetative growth, but also for plant fertility and seed formation.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide identification and characterization of cystatin family genes in rice (Oryza sativa L.)

et al. 2015

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11 Cystatin genes in rice were identified, and their expression patterns were comprehensively analyzed, which reveals multiple roles in both seed development and plant response to environmental variations. Cystatin is a group of small proteins and known to inhibit the activities of cysteine proteases in the papain C1A and legumain C13 peptidase families in plants. Cystatin family genes have only been well characterized recently in a few plant species such as Hordeum vulgare and Nicotiana tabacum, which show their critical roles in programmed cell death and responses to biotic stresses. Up to now, little is known about cystatin family genes and their roles in Oryza sativa, a model plant for cereal biology study. Here, we identified 11 cystatin genes in rice genome. Comprehensive expression profile analysis reveals that cystatin family genes in rice display diverse expression pattern. They are temporally regulated at different developmental stages during the process of seed production and germination. Our experiments also reveal that the majority of cystatin genes are responsive to plant hormones and different environmental cues including cold, drought and other abiotic stresses, while some others are very stable under different stresses, indicating their fundamental roles in normal plant development. In addition, their distribution in rice chromosomes and their evolutionary relation to the members of Cystatin family in A. thaliana and N. tabacum have also been analyzed. These works suggest multiple roles of cystatin family genes in both seed development and plant response to environmental variations.

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A Bipartite Molecular Module Controls Cell Death Activation in the Basal Cell Lineage of Plant Embryos

Abstract: During plant embryogenesis, once the suspensor organ of the plant embryo has fulfilled its role, it is removed by programmed cell death (PCD). The pro-death cathepsin protease NtCP14 initiates this PCD, but is inhibited by the cystatin NtCYS until the suspensor function is fulfilled.

Cited by 73 publications

References 39 publications

Subfamily-Specific Fluorescent Probes for Cysteine Proteases Display Dynamic Protease Activities during Seed Germination

Subfamily-Specific Fluorescent Probes for Cysteine Proteases Display Dynamic Protease Activities during Seed Germination

Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis

Genome-wide identification and characterization of cystatin family genes in rice (Oryza sativa L.)

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