Caspase-Like Activities Accompany Programmed Cell Death Events in Developing Barley Grains

Tran, Vân Nam; Weier, Diana; Radchuk, Ruslana; Thiel, Johannes; Radchuk, Volodymyr

doi:10.1371/journal.pone.0109426

Cited by 35 publications

(34 citation statements)

References 56 publications

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“…It largely degenerates toward maturation while the chlorenchyma layer and crease region remain alive till desiccation (Tran et al, 2014). At the mid stage (as sampled here), it somehow behaves as if it were an autotrophic leaf enveloping the heterotrophic storage organs.…”

Section: The Grain As a Synergistic Metabolic And Architectural Systemmentioning

confidence: 75%

Metabolic architecture of the cereal grain and its relevance to maximize carbon use efficiency

et al. 2015

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Here, we have characterized the spatial heterogeneity of the cereal grain's metabolism and demonstrated how, by integrating a distinct set of metabolic strategies, the grain has evolved to become an almost perfect entity for carbon storage. In vivo imaging revealed light-induced cycles in assimilate supply toward the ear/grain of barley (Hordeum vulgare) and wheat (Triticum aestivum). In silico modeling predicted that, in the two grain storage organs (the endosperm and embryo), the light-induced shift in solute influx does cause adjustment in metabolic flux without changes in pathway utilization patterns. The enveloping, leaf-like pericarp, in contrast, shows major shifts in flux distribution (starch metabolism, photosynthesis, remobilization, and tricarboxylic acid cycle activity) allow to refix 79% of the CO 2 released by the endosperm and embryo, allowing the grain to achieve an extraordinary high carbon conversion efficiency of 95%. Shading experiments demonstrated that ears are autonomously able to raise the influx of solutes in response to light, but with little effect on the steady-state levels of metabolites or transcripts or on the pattern of sugar distribution within the grain. The finding suggests the presence of a mechanism(s) able to ensure metabolic homeostasis in the face of short-term environmental fluctuation. The proposed multicomponent modeling approach is informative for predicting the metabolic effects of either an altered level of incident light or a momentary change in the supply of sucrose. It is therefore of potential value for assessing the impact of either breeding and/or biotechnological interventions aimed at increasing grain yield.Raising the productivity of a given crop genotype requires an increase in the plant's ability to efficiently respond to a changeable environment. At the physiological level, this involves adjustments to the photosynthetic activity of its leaves, to the control of assimilate movement from source to sink, and to the efficiency of assimilate storage. The manipulation of the plant's efficiency to fix carbon, to use energy and nutrients, and to utilize water has been suggested as a route for improving crop productivity (Amthor 2010;De Block and Van Lijsebettens, 2011). Particular attention has been devoted to the cereals, given their central role in the human diet. While the necessary integration of physiological and developmental processes in all plants relies on the transmission of hormonal, metabolic, and other signals through the vascular system (van Bel et al., 2013), this is not the case in the cereal grain, because this network does not extend beyond the pericarp, a maternal structure that encloses the filial storage organs (embryo and endosperm; Radchuk and Borisjuk, 2014). The isolation of the filial from the maternal tissues in the cereal grain creates a complex metabolic system, involving, at the least, a tripartite interaction between the pericarp, endosperm, and embryo. These three grain components in effect form an interactive system of autonomous...

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Section: The Grain As a Synergistic Metabolic And Architectural Systemmentioning

confidence: 75%

Metabolic architecture of the cereal grain and its relevance to maximize carbon use efficiency

et al. 2015

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“…The proteolytic properties of the recombinant VPE4 protein suggest its similar function in plant tissues and thus define the caspase‐1‐like activity at the site of VPE expression in developing barley grains. The VPE4 expression pattern (Radchuk et al ., ) coincides with the profile of caspase‐1‐like activity in the developing pericarp (Tran et al ., ), suggesting that VPE4 may be the major enzyme responsible for the activity in the tissue.…”

Section: Discussionmentioning

confidence: 99%

“…Arabidopsis cathepsin B is vacuolar in proteomic studies (Carter et al ., ), so it would be accessible for VPE action. The coordinated decrease of several caspase‐like activities following VPE4 repression further strengthens an earlier hypothesis (Tran et al ., ) that the co‐action of caspase‐like protease activities is required to execute and/or regulate PCD processes in plant tissues, analogous to those that occur in animal cells (Degterev et al ., ; Shalini et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Vacuolar processing enzyme 4 contributes to maternal control of grain size in barley by executing programmed cell death in the pericarp

et al. 2017

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The angiosperm embryo and endosperm are limited in space because they grow inside maternal seed tissues. The elimination of cell layers of the maternal seed coat by programmed cell death (PCD) could provide space and nutrition to the filial organs. Using the barley (Hordeum vulgare L.) seed as a model, we elucidated the role of vacuolar processing enzyme 4 (VPE4) in cereals by using an RNAi approach and targeting the enzymatic properties of the recombinant protein. A comparative characterization of transgenic versus wild-type plants included transcriptional and metabolic profiling, flow cytometry, histology and nuclear magnetic imaging of grains. The recombinant VPE4 protein exhibited legumain and caspase-1 properties in vitro. Pericarp disintegration was delayed in the transgenic grains. Although the VPE4 gene and enzymatic activity was decreased in the early developing pericarp, storage capacity and the size of the endosperm and embryo were reduced in the mature VPE4-repressed grains. The persistence of the pericarp in the VPE4-affected grains constrains endosperm and embryo growth and leads to transcriptional reprogramming, perturbations in signalling and adjustments in metabolism. We conclude that VPE4 expression executes PCD in the pericarp, which is required for later endosperm filling, and argue for a role of PCD in maternal control of seed size in cereals.

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“…Caspase-1, -3, -4, -6 and -8-like activities have been reported during plant PCD (Cai et al 2014;Tran et al 2014). …”

Section: Execution Of Pcd In Plantsmentioning

confidence: 99%

Programmed cell death: genes involved in signaling, regulation, and execution in plants and animals

Rantong

Gunawardena

2015

Botany

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Programmed cell death (PCD) is a suicide mechanism adopted by multicellular organisms that is essential for development and resistance to different forms of stress. In plants, PCD is involved from embryogenesis to death of the whole plant. PCD is genetically regulated and the molecular pathways involved in different forms of this process in animals are relatively more understood, less is known in plants. At the morphological level, apoptosis, one of the forms of PCD in animals, and plant PCD have some similarities such as cell shrinkage, shrinkage of the nucleus, and DNA fragmentation. Since morphological characteristics are a product of the genetically encoded PCD mechanism, it is of interest to figure out how much of the apoptotic pathway is shared with plant PCD in terms of the genes involved. Evidence of some level of similarities has been gathered in the last decade; including conservation during signaling, regulation and execution of plant PCD and apoptosis. A continued search into the genomes of plants has provided insights about homologues of apoptosis genes present in plants and functional analysis are providing evidence about which genes are carrying out similar roles during apoptosis and plant PCD. This review is aimed at updating on the progress of plant PCD mechanism research and highlighting some of the similarities and differences between plant and mammalian PCD mechanisms, with special focus on the commonalities.

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Caspase-Like Activities Accompany Programmed Cell Death Events in Developing Barley Grains

Cited by 35 publications

References 56 publications

Metabolic architecture of the cereal grain and its relevance to maximize carbon use efficiency

Metabolic architecture of the cereal grain and its relevance to maximize carbon use efficiency

Vacuolar processing enzyme 4 contributes to maternal control of grain size in barley by executing programmed cell death in the pericarp

Programmed cell death: genes involved in signaling, regulation, and execution in plants and animals

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