Suppression of the tonoplast sugar transporter, StTST3.1, affects transitory starch turnover and plant growth in potato

SUMMARY Transitory starch and vacuolar sugars function as highly dynamic pools of instantly accessible metabolites in plant leaf cells. Their metabolic regulation is critical for plant survival. The tonoplast sugar transporters (TSTs), responsible for sugar uptake into vacuoles, regulate cellular sugar partitioning and vacuolar sugar accumulation. However, whether TSTs are involved in leaf transient starch turnover and plant growth is unclear. Here, we found that suppressing StTST3.1 resulted in growth retardation and pale green leaves in potato plants. StTST3.1‐silenced plants displayed abnormal chloroplasts and impaired photosynthetic performance. The subcellular localization assay and the oscillation expression patterns revealed that StTST3.1 encoded a tonoplast‐localized protein and responded to photoperiod. Moreover, RNA‐seq analyses identified that starch synthase (SS2 and SS6) and glucan water, dikinase (GWD), were downregulated in StTST3.1‐silenced lines. Correspondingly, the capacity for starch synthesis and degradation was decreased in StTST3.1‐silenced lines. Surprisingly, StTST3.1‐silenced leaves accumulated exceptionally high levels of maltose but low levels of sucrose and hexose. Additionally, chlorophyll content was reduced in StTST3.1‐silenced leaves. Analysis of chlorophyll metabolic pathways found that Non‐Yellow Coloring 1 (NYC1)‐like (NOL), encoding a chloroplast‐localized key enzyme that catalyzes the initial step of chlorophyll b degradation, was upregulated in StTST3.1‐silenced leaves. Transient overexpression of StNOL accelerated chlorophyll b degradation in tobacco leaves. Our results indicated that StTST3.1 is involved in transitory starch turnover and chlorophyll metabolism, thereby playing a critical role in normal potato plant growth. Significance Statement Our work demonstrates that the tonoplast sugar transporter StTST3.1 plays a critical role in starch degradation by affecting maltose metabolism, providing new insight into the starch turnover pathway in plant leaves.