Over-activation of cold tolerance in arabidopsis causes carbohydrate shortage compared with Chorispora bungeana.

Many plants cope with cold stress by developing acquired freezing tolerance (AFT) through cold acclimation (CA), and some species have strong basal freezing tolerance (BFT) independent of CA. Although CA has been extensively studied, its potential in agricultural applications is still unclear. Here, carbohydrate metabolism and transcriptome in AFT plant Arabidopsis and BFT plant Chorispora bungeana were compared with each other. The results showed that, although both species were able to accumulate soluble sugars during CA, leaf starch accumulation in the daytime was almost blocked in Arabidopsis while it was greatly enhanced in C. bungeana, revealing that Arabidopsis experienced carbohydrate shortage during CA. Transcriptome and pathway enrichment analysis found that genes for photosynthesis antenna proteins were generally repressed by cold stress in both species. However, cold-up-regulated genes were enriched in protein translation in Arabidopsis, whilst they were enriched in carotenoid biosynthesis, flavonoid biosynthesis, and beta-amylases in C. bungeana. Furthermore, weighted gene co-expression network analysis (WGCNA) showed that the inhibition of starch accumulation was associated with down-regulation of genes for photosynthesis antenna proteins and up-regulation of genes for protein translation, DNA repair, and proteasome in Arabidopsis but not in C. bungeana. Taken together, our results revealed that over-activation of common tolerant mechanisms resulted in insufficient carbohydrate supplies in Arabidopsis during CA, and photoprotective mechanisms played important roles in cold adaptation of C. bungeana. These findings uncovered the drawback of CA in improving freezing tolerance and highlighted photoprotection as a possible solution for agricultural applications.

Comparison with Arabidopsis reveals optimal nitrogen allocation strategy and mechanism in Chorispora bungeana, a cryophyte with strong freezing tolerance.

The stress responses of plant compete for resources with growth and development. Resource allocations among these processes may have been optimized in plants adapted to natural habitats. Here, nitrogen (N) allocations were compared in leaves of Arabidopsis and Chorispora bungeana, a cryophyte with strong freezing tolerance. The results showed that the two species differed not only in N partitions among N forms and allocations among leaves, but also in their responses to cold stress. Interestingly, leaf protein contents were enhanced in C. bungeana while reduced in Arabidopsis, though the N allocations to leaves were reduced in both plants upon cold stress. Profoundly, when grown at warm temperature, contents of total free amino acids (FAAs) in leaves of C. bungeana were 6-11 times higher than those in Arabidopsis. In contrast, cold treatment induced FAAs accumulation in leaves of Arabidopsis without having significant effect in any leaf of C. bungeana. Considerable discrepancy was also found between the two species in the expressions of nitrate transporter genes and the activities of nitrate assimilation enzymes. Correlation and network analysis showed that most NPFs were clustered in a single network module and had loose relations with protein synthesis in Arabidopsis, while they were distributed in different modules in a decentralized network in C. bungeana. Therefore, our results reveal that C. bungeana may have optimized its N allocation strategy by producing and storing amino acids as efficient N reserve and adopting a decentralized network for N utilization, which may equip the plant with powerful capabilities for environmental adaptions.

A cold-induced pectin methyl-esterase inhibitor gene contributes negatively to freezing tolerance but positively to salt tolerance in Arabidopsis.

Plant pectin methyl-esterase (PME) and PME inhibitor (PMEI) belong to large gene families whose members are proposed to be widely involved in growth, development, and stress responses; however, the biological functions of most PMEs and PMEIs have not been characterized. In this study, we studied the roles of CbPMEI1, a cold-induced pectin methyl-esterase inhibitor (PMEI) gene from Chorispora bungeana, under freezing and salt stress. The putative CbPMEI1 peptide shares highest similarity (83%) with AT5G62360 (PMEI13) of Arabidopsis. Overexpression of either CbPMEI1 or PMEI13 in Arabidopsis decreased tissue PME activity and enhanced the degree of methoxylation of cell wall pectins, indicating that both genes encode functional PMEIs. CbPMEI1 and PMEI13 were induced by cold but repressed by salt stress and abscisic acid, suggesting distinct roles of the genes in freezing and salt stress tolerance. Interestingly, transgenic Arabidopsis plants overexpressing CbPMEI1 or PMEI13 showed decreased freezing tolerance, as indicated by survival and electrolyte leakage assays. On the other hand, the salt tolerance of transgenic plants was increased, showing higher rates of germination, root growth, and survival under salinity conditions as compared with non-transgenic wild-type plants. Although the transgenic plants were freezing-sensitive, they showed longer roots than wild-type plants under cold conditions, suggesting a role of PMEs in balancing the trade-off between freezing tolerance and growth. Thus, our study indicates that CbPMEI1 and PMEI13 are involved in root growth regulation under cold and salt stresses, and suggests that PMEIs may be potential targets for genetic engineering aimed to improve fitness of plants under stress conditions.