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VaAPL1 Promotes Starch Synthesis to Constantly Contribute to Soluble Sugar Accumulation, Improving Low Temperature Tolerance in Arabidopsis and Tomato.

ABSTRACT: ADP-glucose pyrophosphorylase (AGPase) is a key rate-limiting enzyme involved in starch synthesis. APL1, an AGPase large subunit, plays an important role in the growth and development of grapes; however, its function in withstanding low temperature (LT) remains elusive. Hence, VaAPL1 was cloned from Vitis amurensis (Zuoshan I), and its function was characterized. The gene was highly expressed in the phloem of V. amurensis during winter dormancy (0, -5, and - 10°C). Phylogenetic relationships demonstrated that VaAPL1 was closely genetic related to SlAPL1 (from Solanum lycopersicum), and clustered into I group. Further, VaAPL1 was ectopically expressed in Arabidopsis thaliana (ecotype Columbia, Col) and tomato ("Micro-Tom" tomato) to characterize its function under LT. Compared with Col, the average survival rate of VaAPL1-overexpressing A. thaliana exceeded 75.47% after freezing treatment. Moreover, reactive oxygen species (ROS) content decreased in VaAPL1-overexpressing A. thaliana and tomato plants under LT stress. The activities of AGPase, and starch contents in VaAPL1-overexpressing A. thaliana were higher than in Col after LT stress. The contents of sucrose and glucose were accumulated in overexpressing plants compared with wild-type at 0 h and 24 h after LT stress. Transcriptome sequencing of overexpressing tomato plants revealed involvement in sugar metabolism and the hormone signal pathway, and Ca²⁺ signaling pathway-related genes were up-regulated. Hence, these results suggest that overexpression of VaAPL1 not only ensured sufficient starch converting into soluble sugars to maintain cell osmotic potential and provided energy, but also indirectly activated signal pathways involved in LT to enhance plant tolerance.

SUBMITTER: Liang G

PROVIDER: S-EPMC9257282 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundStarch is the predominant storage compound in underground plant tissues like roots and tubers. An exception is sugar beet tap-root (Beta vulgaris ssp altissima) which exclusively stores sucrose. The underlying mechanism behind this divergent storage accumulation in sugar beet is currently not fully known. From the general presence of starch in roots and tubers it could be speculated that the lack in sugar beet tap-roots would originate from deficiency in pathways leading to starch. Therefore with emphasis on starch accumulation, we studied tap-roots of sugar beet using parsnip (Pastinaca sativa) as a comparator.ResultsMetabolic and structural analyses of sugar beet tap-root confirmed sucrose as the exclusive storage component. No starch granules could be detected in tap-roots of sugar beet or the wild ancestor sea beet (Beta vulgaris ssp. maritima). Analyses of parsnip showed that the main storage component was starch but tap-root tissue was also found to contain significant levels of sugars. Surprisingly, activities of four main starch biosynthetic enzymes, phosphoglucomutase, ADP-glucose pyrophosphorylase, starch synthase and starch branching enzyme, were similar in sugar beet and parsnip tap-roots. Transcriptional analysis confirmed expression of corresponding genes. Additionally, expression of genes involved in starch accumulation such as for plastidial hexose transportation and starch tuning functions could be determined in tap-roots of both plant species.ConclusionConsidering underground storage organs, sugar beet tap-root upholds a unique property in exclusively storing sucrose. Lack of starch also in the ancestor sea beet indicates an evolved trait of biological importance.Our findings in this study show that gene expression and enzymatic activity of main starch biosynthetic functions are present in sugar beet tap-root during storage accumulation. In view of this, the complete lack of starch in sugar beet tap-roots is enigmatic.

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VaAPL1 Promotes Starch Synthesis to Constantly Contribute to Soluble Sugar Accumulation, Improving Low Temperature Tolerance in Arabidopsis and Tomato.

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