Physiological, metabolic, and stomatal adjustments in response to salt stress in Jatropha curcas.

Salinity is a major issue affecting photosynthesis and crop production worldwide. High salinity induces both osmotic and ionic stress in plant tissues as a result of complex interactions among morphological, physiological, and biochemical processes. Salinity, in turn, can provoke inactivation of some enzymes in the Calvin-Benson cycle and therefore affect the fine adjustment of electron transport in photosystem I and carbon related reactions. Here, we used three contrasting Jatropha curcas genotypes namely CNPAE183 (considered tolerant to salinity), CNPAE218 (sensible), and JCAL171 (intermediate) to understand salinity responses. By performing a long-term (12 months) experiment in land conditions, we investigated distinct mechanisms used by J. curcas to cope with threatening salinity effects by analyzing gas exchange, mineral nutrition and metabolic responses. First, our results highlighted the plasticity of stomatal development and density in J. curcas under salt stress. It also demonstrated that the CNPAE183 presented higher salt-tolerance whereas CNPAE218 displayed a more sensitive salt-tolerance response. Our results also revealed that both tolerance and sensitivity to salinity were connected with an extensive metabolite reprogramming in the Calvin-Benson cycle and Tricarboxylic Acid cycle intermediates with significant changes in amino acids and organic acids. Collectively, these results indicate that the CNPAE183 and CNPAE218 genotypes demonstrated certain characteristics of salt-tolerant-like and salt-sensitive-like genotypes, respectively. Overall, our results highlight the significance of metabolites associated with salt responses and further provide a useful selection criterion in during screening for salt tolerance in J. curcas in breeding programmes. Schematic summary model showing metabolic and physiologic responses to salt (NaCl) and plant mitochondria and chloroplast in J. curcas. Ions Na+ and Cl− were translocated by leaves through xylem. In the leaves, these ions provokes NaCl stress symptoms triggering oxidative ionic and osmotic stress on cells. Once inside the chloroplast the Na+ ions provokes downregulation of many Calvin-Benson cycle enzymes (e.g. Rubisco, Fructose 1,6-bisphosphatase, Sedoheptulose 1,7-bisphosphatase, transketolase, Ribulose 5-phosphate isomerase)1. This leads to the inhibition of the conversion of ribose 5-phosphate to Ribulose 5-phosphate by Ribulose 5-Phosphate Isomerase and ultimately to the downregulation of photosynthesis only in J. curcas salt-sensitive like plants (here referred as CNPAE183). Notably, in J. curcas salt-tolerant like plants (here referred as CNPAE218) a maintenance of photosynthesis occurs and it resulted in healthy foliage and fruiting. Once in mitochondria, Na+ ions appears to stimulate a complex metabolic reprograming that involved enhanced glycolysis, increase on the tricarboxylic cycle acid intermediates coupled with the synthesis of amino acids and organic acids. Abbreviations: TCA, tricarboxylic acid cycle; 1 = downregulation of Calvin-Benson cycle enzymes proposed by Lin et al. (2018) and Sivakumar et al. (2000). [Display omitted] • Jatropha curcas used combined protection mechanism to stabilize photosystems; • Differential changes promoted by tolerant-like plants may help to select elite genotypes; • Stomata regulate the transpiration force affecting physiological responses; • CNPAE218 is a promising candidate in the plant breeding based on its responses; [ABSTRACT FROM AUTHOR]