24Plants undergo several developmental transitions during their life cycle. One of these, the 25 differentiation of the young embryo from a meristem-like structure into a highly-specialized 26 storage organ, is vital to the formation of a viable seed. For crops in which the seed itself is the 27 end product, effective accumulation of storage compounds is of economic relevance, defining 28 the quantity and nutritive value of the harvest yield. However, the regulatory networks 29 underpinning the phase transition into seed filling are poorly understood. Here we show that 30 trehalose 6-phosphate (T6P), which functions as a signal for sucrose availability in plants, 31 mediates seed filling processes in seeds of the garden pea (Pisum sativum), a key grain legume.
32Seeds deficient in T6P are compromised in size and starch production, resembling the wrinkled 33 seeds studied by Gregor Mendel. We show also that T6P exerts these effects by stimulating the 34 biosynthesis of the pivotal plant hormone, auxin. We found that T6P promotes the expression 35 of the auxin biosynthesis gene TRYPTOPHAN AMINOTRANSFERASE RELATED2 (TAR2), 36 and the resulting effect on auxin levels is required to mediate the T6P-induced activation of 37 storage processes. Our results suggest that auxin acts downstream of T6P to facilitate seed 38 filling, thereby providing a salient example of how a metabolic signal governs the hormonal 39 control of an integral phase transition in a crop plant.40 41 Keywords 42 Trehalose 6-phosphate, auxin, sugar signaling, embryo development, seed filling, starch 43 biosynthesis, pea 44 45 Introduction 46 The transition from early patterning into seed filling is an important phase change in developing 47 seeds, ensuring seed survival and the nourishment of seedling growth upon germination. For 48 this reason, plants have evolved a regulatory network to control seed filling, and carbohydrates 49 appear to play a pivotal role in this process (Weber et al., 2005; Hills, 2004). Sucrose is thought 50 to have a dual function in developing seeds as a nutrient sugar and as a signal molecule 51 triggering storage-associated gene expression (Weber et al., 1998). Two decades ago, the 52 invertase control hypothesis of seed development was formulated, suggesting that seed coat-53 borne invertases prevent the onset of storage processes in the early embryo by cleaving the 54 incoming sucrose into hexoses (Weber et al., 1995a). When invertase activity declines, sucrose 55 levels begin to rise and seed filling is initiated. However, relatively little is known about the 56 perception and signaling of this metabolic switch. 57 T6P, the intermediate of trehalose biosynthesis, has been shown to be an essential signal 58 metabolite in plants, linking growth and development to carbon metabolism (Lunn et al., 2006; 59 Figueroa et al., 2016b). The sucrose-T6P nexus model postulates that T6P acts as a signal of 60 sucrose availability, helping to maintain sucrose levels within a range that is appropriate for the 61 developmental st...