Abstract
Despite the relevance of seed-filling mechanisms for crop yield, we still have only a rudimentary understanding of the transport processes that supply the caryopsis with sugars. We hypothesized that SWEET sucrose transporters may play important roles in nutrient import pathways in the rice caryopsis. We used a combination of mRNA quantification, histochemical analyses, translational promoter-reporter fusions and analysis of knockout mutants created by genomic editing to evaluate the contribution of SWEET transporters to seed filling. In rice caryopses, SWEET11 and 15 had the highest mRNA levels and proteins localized to four key sites: all regions of the nucellus at early stages; the nucellar projection close to the dorsal vein; the nucellar epidermis that surrounds the endosperm; and the aleurone. ossweet11;15 double knockout lines accumulated starch in the pericarp, whereas caryopses did not contain a functional endosperm. Jointly, SWEET11 and 15 show all the hallmarks of being necessary for seed filling with sucrose efflux functions at the nucellar projection and a role in transfer across the nucellar epidermis/aleurone interface, delineating two major steps for apoplasmic seed filling, observations that are discussed in relation to observations made in rice and barley regarding the relative prevalence of these two potential import routes.
Highlights
Population growth is expected to lead to an increasing need for rice production, especially in Africa (Sharma, 2014)
The microarray showed that OsSWEET15 was only 2–39 lower compared to OsSWEET11, our analysis indicated a much lower relative level
We draw five key conclusions from the results of a combination of analyses comprising gene expression, translational reporters to map tissue-specific protein accumulation, and knockout mutants (a) that were generated by genome editing: (1) OsSWEET11 and 15 are the most highly expressed sucrose transporting SWEETs in the rice caryopsis; (2) if we assume that they mark apoplasmic import routes, sucrose can enter both directly below the vein via the nucellar projection as well as via the circumferential nucellar epidermis; (3) SWEET11 and 15 may play roles in cellular efflux at these two sites, but may be responsible for importing sucrose into the aleurone; (4) OsSWEET11 and 15 both contribute to seed filling with seemingly redundant roles
Summary
Population growth is expected to lead to an increasing need for rice production, especially in Africa (Sharma, 2014). Rice grains are composed mainly of starch (over 90% in many cases; www.knowledgebank.irri.org/ricebreedingcourse/Grain_ quality.htm), which derives from imported soluble carbohydrates. These carbohydrates are produced and delivered from leaves (source tissues) to caryopses (sink tissues) via the phloem (Patrick, 1997; Patrick & Offler, 2001). Sucrose is unloaded from the phloem strands that enter the seed coat, from where sugars are transferred into the developing caryopsis to supply cells with nutrients, in particular sugars as sources of energy and as carbon skeletons for cell wall and starch biosynthesis (Oparka & Gates, 1984; Patrick & Offler, 2001; Zhang et al, 2007)
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