Manipulation of sucrose phloem and embryo loading affects pea leaf metabolism, carbon and nitrogen partitioning to sinks as well as seed storage pools

Abstract

SummarySeed development largely depends on the long‐distance transport of sucrose from photosynthetically active source leaves to seed sinks. This source‐to‐sink carbon allocation occurs in the phloem and requires the loading of sucrose into the leaf phloem and, at the sink end, its import into the growing embryo. Both tasks are achieved through the function of SUT sucrose transporters. In this study, we used vegetable peas (Pisum sativum L.), harvested for human consumption as immature seeds, as our model crop and simultaneously overexpressed the endogenous SUT1 transporter in the leaf phloem and in cotyledon epidermal cells where import into the embryo occurs. Using this ‘Push‐and‐Pull’ approach, the transgenic SUT1 plants displayed increased sucrose phloem loading and carbon movement from source to sink causing higher sucrose levels in developing pea seeds. The enhanced sucrose partitioning further led to improved photosynthesis rates, increased leaf nitrogen assimilation, and enhanced source‐to‐sink transport of amino acids. Embryo loading with amino acids was also increased in SUT1‐overexpressors resulting in higher protein levels in immature seeds. Further, transgenic plants grown until desiccation produced more seed protein and starch, as well as higher seed yields than the wild‐type plants. Together, the results demonstrate that the SUT1‐overexpressing plants with enhanced sucrose allocation to sinks adjust leaf carbon and nitrogen metabolism, and amino acid partitioning in order to accommodate the increased assimilate demand of growing seeds. We further provide evidence that the combined Push‐and‐Pull approach for enhancing carbon transport is a successful strategy for improving seed yields and nutritional quality in legumes.

Far‐red radiation stimulates dry mass partitioning to fruits by increasing fruit sink strength in tomato

“…Photosynthetic assimilates (sucrose) unloading from the phloem to the sink is usually facilitated symplasmically by sugar transporters (Carpaneto et al ., 2005; Chen et al ., 2012). For example, sugar transporter activities positively correlate with sugar accumulation in pea (Lu et al ., 2019), Arabidopsis (Gottwald et al ., 2000), tobacco (Bürkle et al ., 1998) and maize (Slewinski et al ., 2009). Upon transportation into sinks, sucrose can be degraded into glucose, fructose, or other derivatives (Ruan, 2014).…”

Role of ureides in source-to-sink transport of photoassimilates in non-fixing soybean

“… Herman, 2014 ; Santiago and Tegeder, 2016 , 2017 ). Similar, multifaceted adjustments in the C and N (and/or sulfur) household and source-to-sink transport have been observed in pea when phloem loading of amino acids or sucrose was up-regulated ( Zhang et al , 2015 ; Lu et al , 2020 ), potentially hinting at the presence of a common scheme of signaling, sensing, and modifying the C/N balance upstream of C and N phloem loading.…”

“…Total ureides, allantoin, and allantoic acid levels were analyzed according to Collier and Tegeder (2012) using 5 mg of lyophilized tissues or 25 µl and 300 µl of undiluted xylem sap and leaf phloem exudates, respectively. Amino acids were extracted and derivatized with 4-fluoro-7-nitro-2,1,3-benzoxadiazole (NBD-F) as previously described ( Aoyama et al , 2004 ), and HPLC was performed following Lu et al (2020) .…”

Multi-gene metabolic engineering of tomato plants results in increased fruit yield up to 23%

“…This suggests that the photosynthetic activity of source tissues is controlled either by the metabolism of photoassimilates within source tissue, insufficient sink strength or inhibition of their transport 64 . This hypothesis is further supported by experiments in potato and pea which indicate that transgenic manipulation of both source and sink is a highly effective route for enhancing the harvest index of a crop species 39,48 . Recently, a multi-transgenic approach has been used that targeted both C and N metabolism was proven to be effective in enhancing Arabidopsis growth 65 .…”

“…This is mainly due to signals that communicate and regulate the mechanisms of shifting C flow between source and sink tissues. The potential of this strategy is demonstrated by the only experiments to date to make targeted manipulations of both source and sink 39,48 . First, expression of transgenes in potato leaves to increase the partitioning of photoassimilates towards sucrose and away from starch was combined with over expression of two transporters to increase the capacity for starch storage in the tuber 39 .…”