Abstract
Programmed cell death (PCD) is one of the most intensively researched fields in modern mammalian biology with roles in cancer, aging, diabetes and numerous neurodegenerative diseases. It is becoming increasingly clear that PCD also plays significant roles in plant defence and responses to the environment. Given their unique ability to tolerate desiccation (cells remain viable even after they’ve lost 95% of their water), resurrection plants make ideal models to study the regulation of plant PCD pathways. Previously, we showed that the Australian resurrection plant, Tripogon loliiformis, suppresses plant PCD, via trehalose-mediated activation of autophagy pathways, during drying. In the present study, we created a full-length T. loliiformis cDNA library, performed a large-scale Agrobacterium screen for improved salinity tolerance and identified Stachyose synthase (TlStach) as a potential candidate for improving stress tolerance. Tripogon loliiformis shoots accumulate stachyose synthase transcripts and stachyose during drying. Attempts to generate transgenic plants expressing TlStach failed and were consistent with previous reports in mammals that demonstrated stachyose-mediated induction of apoptosis. Using a combination of transcriptomics, metabolomics and cell death assays (TUNNEL and DNA laddering), we investigated whether stachyose induces apoptotic-like cell death in T. loliiformis. We show that stachyose triggers the formation of the hallmarks of plant apoptotic-like cell death in the desiccation sensitive Nicotiana benthamiana but not the resilient T. loliiformis. These findings suggest that T. loliiformis suppresses stachyose-mediated apoptotic-like cell death and provides insights on the role of sugar metabolism and plant PCD pathways. A better understanding of how resilient plants regulate sugar metabolism and PCD pathways may facilitate future targeting of plant metabolic pathways for increased stress tolerance.
Highlights
Programmed cell death (PCD) is one of the most intensively researched fields in modern mammalian biology with roles in cancer, aging, diabetes and numerous neurodegenerative diseases
Using a Full‐length cDNA Over‐eXpressing (FOX) screen of a T. loliiformis cDNA in Agrobacterium subjected to salinity stress, we identified a stress-induced stachyose synthase
Exogenous application of stachyose induced typical apoptotic hallmarks, including DNA laddering and nuclear fragmentation in N. benthamiana plants but not in T. loliiformis plants. These results suggest that T. loliiformis encodes, and implements, measures that suppress stachyose-induced apoptotic cell death and may highlight potential gene targets for the suppression of plant PCD pathways and the production of stress-tolerant crops
Summary
Programmed cell death (PCD) is one of the most intensively researched fields in modern mammalian biology with roles in cancer, aging, diabetes and numerous neurodegenerative diseases. It is becoming increasingly clear that PCD plays significant roles in plant defence and responses to the environment Given their unique ability to tolerate desiccation (cells remain viable even after they’ve lost 95% of their water), resurrection plants make ideal models to study the regulation of plant PCD pathways. We show that stachyose triggers the formation of the hallmarks of plant apoptotic-like cell death in the desiccation sensitive Nicotiana benthamiana but not the resilient T. loliiformis These findings suggest that T. loliiformis suppresses stachyose-mediated apoptotic-like cell death and provides insights on the role of sugar metabolism and plant PCD pathways. Researchers have significant knowledge of the drought responses of economically important crops; far less information is available on the molecular and metabolic strategies used by resurrection plants to cope with desiccation. In FOX gene hunting, libraries of cDNAs are inserted into expression cassettes and transformed into a model plant system such as Arabidopsis where they are screened directly for the trait of interest[10]
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