Trehalose 6‐phosphate promotes seed filling by activating auxin biosynthesis

Abstract

Plants undergo several developmental transitions during their life cycle. One of these, the differentiation of the young embryo from a meristem-like structure into a highly specialized storage organ, is believed to be controlled by local connections between sugars and hormonal response systems. However, we know little about the regulatory networks underpinning the sugar-hormone interactions in developing seeds. By modulating the trehalose 6-phosphate (T6P) content in growing embryos of garden pea (Pisum sativum), we investigate here the role of this signaling sugar during the seed-filling process. Seeds deficient in T6P are compromised in size and starch production, resembling the wrinkled seeds studied by Gregor Mendel. We show also that T6P exerts these effects by stimulating the biosynthesis of the pivotal plant hormone, auxin. We found that T6P promotes the expression of the auxin biosynthesis gene TRYPTOPHAN AMINOTRANSFERASE RELATED2 (TAR2), and the resulting effect on auxin concentrations is required to mediate the T6P-induced activation of storage processes. Our results suggest that auxin acts downstream of T6P to facilitate seed filling, thereby providing a salient example of how a metabolic signal governs the hormonal control of an integral phase transition in a crop plant.

OsTPP1 regulates seed germination through the crosstalk with abscisic acid in rice

“…Meanwhile, the content of trehalose gradually decreased from 12 h to 24 h, which probably modulated seed germination through maintaining sucrose state as reported in other developmental stages (Lunn et al ., 2006; Yadav et al ., 2014; Meitzel et al ., 2020). The sucrose concentrations of the two lines also were measured at 12 h and 24 h postimbibition.…”

“…The tpp1 mutant showed reduced trehalose content and altered sucrose concentration during seed germination, indicating that the OsTPP1 gene potentially influenced the starch‐to‐sucrose conversion during seed germination. This finding further provided evidence for the dual function of sucrose as a key metabolite and signaling molecule during different developmental stages (Weber et al ., 2005; Meitzel et al ., 2020). mRNA transcripts or hormones could have been accumulated in seeds during late stages of seed maturation, and subsequently may either degrade (reducing dormancy maintenance) or become active (promoting germination) during imbibition (Dure & Waters, 1965).…”

“…Trehalose is finally converted to two molecules of glucose by trehalose (Elbein et al ., 2003; Venturini et al ., 2013). T6P is an essential signal metabolite in plants, linking growth and development to carbon metabolism, and acts as a signal of sucrose status in different developmental stages of the plant (Lunn et al ., 2006; Yadav et al ., 2014; Meitzel et al ., 2020). The TPS genes have been investigated widely in the model plant Arabidopsis and found to be involved in seed germination, stress signaling, vegetative phase change, shoot branching and flowing time control, which mainly referred to TPS1 (Avonce et al ., 2004; Gómez et al ., 2010; Wahl et al ., 2013; Fichtner et al ., 2020a,b; Ponnu et al ., 2020).…”

Regulation of shoot branching in arabidopsis by trehalose 6‐phosphate

“…In addition, there are several lines of evidence that Tre6P associated changes in bud metabolism might also have an impact on auxin synthesis and signalling. Tre6P promotes the expression of the auxin biosynthesis gene TRYPTOPHAN AMINOTRANSFERASE RELATED2 in pea seeds (Meitzel et al ., 2021) and PINOID1 (PIN1) auxin efflux proteins become delocalized in meristems when plants have low C status (Lauxmann et al ., 2016) and therefore low Tre6P levels (Lunn et al ., 2006).…”

How Do Smut Fungi Use Plant Signals to Spatiotemporally Orientate on and In Planta?

“…Another distinct event in the plant life cycle, which might induce teliospore formation, is fertilization leading to embryo formation and seed filling. Here also, carbohydrate signaling and phytohormones direct plant development and seed filling [75]. In summary, little is known about signals governing where and when to sporulate.…”