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Mendel's bequest advanced the understanding of regulatory systems for controlling sugar supply to developing plant embryos

Year: 2008
Type: article
Abstract: Over the past 15 years, a lot of progress has been made in identifying and characterizing genes and proteins involved in the transport of photosynthetically produced sugars from leaves to sink organs such as roots, flowers, and developing seeds. A major step forward was the identification and characterization of genes encoding proton sucrose co-transporters of the SUT family (Riesmeier et al., 1992, 1993, 1994). Strong evidence suggests that SUTs are responsible for the import of sucrose present in the cell wall space of leaves into the phloem conduit (the phloem or the sieve element companion cell complex, SECCC). Moreover, they appear to be responsible for the import of sugars into developing seeds (Weber et al., 1997; Matsukura et al., 2000; Rosche et al., 2002; Baud et al., 2005). However, major pieces of the puzzle are still missing, including the proteins responsible for efflux in the path of sucrose from the leaf palisade parenchyma, where sucrose is synthesized, to the phloem; as well as in sucrose delivery from the phloem in the sink organ to the developing embryo and how the leaf co-ordinates supply with demand at the other end, i.e. the embryo. More importantly, we have very little information on the networks that co-ordinate source supply (here the leaf) with sink demand (here the seed). In parallel to the identification of the actual transporter genes, the laboratories of John Patrick and Tina Offler in Newcastle advanced legume seeds as a model for studying nutrient transfer from the maternal tissue to the developing embryos. This system is ideal since it allows direct monitoring of nutrient transfer by using the ‘empty seed technique’, that is the efflux of nutrients from the seed coat. They found a fascinating induction of cell wall ingrowths that enhance the surface area of the plasma membrane of the cotyledons, which is probably necessary for sustaining the high rates of nutrient flux into the pea embryo (Wardini et al., 2007b). Moreover, Patrick's laboratory developed the ‘split seed technology’ for pea, which enables them to correlate growth, uptake, and gene expression in the same material. Using this system, they demonstrated that the above-mentioned cell wall ingrowths are induced by sugars (Wardini et al., 2007a, b). Using pea as a model system, they showed that pea SUT sucrose transporters are probably crucial players for the uptake of sugars into developing seeds (Harrington et al., 1997a, b; Patrick and Offler, 2001; Rosche et al., 2002). Recently, they made a fascinating discovery when they characterized seed coat-expressed sucrose transporter genes. Most notably, Patrick's group recently identified a set of sucrose transporter homologues called SUFs (sucrose facilitators) that had apparently lost the coupling of sucrose transport to protons, a feature common to all other known members of the SUT family. SUFs are therefore candidates for a function in facilitating efflux from the seed coat along the concentration gradient into the space surrounding the embryo (Zhou et al., 2007b). SUFs are closely related based on their sequences to proton-coupled SUT sucrose transporters, but do not appear to form a separate clade. From a large number of observations, Patrick suggests that enhanced uptake of sugars by filial tissues leads to a decrease in osmolality of the seed apoplasmic sap resulting in an increase in the turgor of seed coat cells (Patrick and Offler, 2001). When the turgor of the seed coat exceeds a ‘set point’, a regulatory system (turgor-homeostat model) activates the efflux transporters in the seed coat in order to meet the demand of the embryo. Under conditions of sustained nutrient demand, the turgor set point decreases to enable higher rates of phloem import (de Jong et al., 1996; Zhang et al., 1996). In this context, Patrick's group and their collaborators found that several aquaporins are expressed in the seed coat, thus representing potential players in controlling water transport and thus the control of turgor (Zhou et al., 2007a). To address the role of sugars as signals that regulate sugar flux and their effect on expression and activity of the SUT and SUF transporters in regulating seed growth and development, Tina Offler and John W Patrick joined forces with Trevor Wang and Cliff Hedley, key players in the characterization of pea seed mutants. The concept of the study presented in this issue of the Journal of Experimental Botany was that a defect in sugar accumulation and in the growth rate of pea seed mutants might be an elegant way to identify the role of sugars in controlling the import into the developing embryo (Zhou et al., 2009). The authors present a careful comparison of wild type (round-seeded) and wrinkled-seeded mutants of pea; mutants that Gregor Mendel used for developing his concept of Mendelian inheritance (Mendel, 1865). The original rugosus (r) locus (rugosus meaning wrinkled in Latin) described by Gregor Mendel in the 19th century and given the gene symbol, r, by White (Mendel, 1865; White, 1917) is caused by a transposon-like insertion in a gene encoding one of the isoforms of the starch branching enzyme (SBEI; Bhattacharyya et al., 1990). The decrease in enzyme activity in the mutant brings about a lower amylopectin/amylose ratio with the amylose content increased to 70% (wild type normally at c. 30%; Wang et al., 1998). Overall, the starch content is reduced in the mutants, while lipid, protein, and free sugar content is increased, leading to a higher osmotic pressure and subsequent higher water uptake. Later on, during seed maturation, the seeds of the pea mutants lose a higher proportion of water relative to the wild type and become wrinkled. Patrick's laboratory developed a hypothesis that describes how the developing embryo communicates demand for carbohydrates to the maternal tissue. Here they test whether and how a defect in starch biosynthesis (with a reduced demand for carbohydrates) affects growth rates of the seeds, expression of SUT and SUF sucrose transporter genes, as well as sugar accumulation with the aim of identifying the nature of the signal used to acclimate transport to use/demand. Through a series of correlations (growth rate versus sucrose uptake, sucrose uptake versus SUT1/SUF1/SUF4 expression, SUT1/SUF1/SUF4 expression versus glucose/sucrose intracellular concentration, and sucrose uptake versus glucose/sucrose intracellular concentration) they observe that expression of SUT1 correlates best with sucrose uptake rates in mutant and wild type. Moreover, since sucrose transport activity as well as SUT1 expression correlate negatively with sucrose levels in the seeds, sucrose itself appears to serve as a signal that affects SUT1 activity through a transcriptional regulatory mechanism. Thus the embryo, uses a negative feedback loop to repress sucrose uptake when the demand is low. As one may have expected, regulation of uptake represents a strategic target of control networks that will have to be worked out in detail. The characterization of mutants deficient in SUT1 function or carrying mutations in the promoter of SUT1 will help to test this hypothesis and will provide a framework for biotechnological approaches aimed at improving yield potential. Regulation of sugar uptake is best understood in the yeast Saccharomyces cerevisiae. In yeast, several plasma membrane localized sensors are used to fine tune the expression of glucose transporters through at least two counteracting negative feedback loops (Kim and Johnston, 2006). It will thus be interesting to see whether plant cells use similar regulatory network logics as well as similar mechanisms to control the uptake of sugars.
DOI: 10.1093/jxb/ern358
Language: English
Subfield: Plant Science
Open Access status: bronze
OpenAlex ID: W2133590365
FWCI: 3.628
Cites: 24
Cited by: 19
Related to: 10