Increased Phloem Transport of S-Methylmethionine Positively Affects Sulfur and Nitrogen Metabolism and Seed Development in Pea Plants

Abstract

Seeds of grain legumes are important energy and food sources for humans and animals. However, the yield and quality of legume seeds are limited by the amount of sulfur (S) partitioned to the seeds. The amino acid S-methylmethionine (SMM), a methionine derivative, has been proposed to be an important long-distance transport form of reduced S, and we analyzed whether SMM phloem loading and source-sink translocation are important for the metabolism and growth of pea (Pisum sativum) plants. Transgenic plants were produced in which the expression of a yeast SMM transporter, S-Methylmethionine Permease1 (MMP1, YLL061W), was targeted to the phloem and seeds. Phloem exudate analysis showed that concentrations of SMM are elevated in MMP1 plants, suggesting increased phloem loading. Furthermore, expression studies of genes involved in S transport and metabolism in source organs, as well as xylem sap analyses, support that S uptake and assimilation are positively affected in MMP1 roots. Concomitantly, nitrogen (N) assimilation in root and leaf and xylem amino acid profiles were changed, resulting in increased phloem loading of amino acids. When investigating the effects of increased S and N phloem transport on seed metabolism, we found that protein levels were improved in MMP1 seeds. In addition, changes in SMM phloem loading affected plant growth and seed number, leading to an overall increase in seed S, N, and protein content in MMP1 plants. Together, these results suggest that phloem loading and source-sink partitioning of SMM are important for plant S and N metabolism and transport as well as seed set.

Phloem-Specific Methionine Recycling Fuels Polyamine Biosynthesis in a Sulfur-Dependent Manner and Promotes Flower and Seed Development

“…AdoMet itself is a major component of Arabidopsis phloem sap (Bourgis et al, 1999). SMM is the phloem-mobile transport form of Met and has a major role for S supply of sink tissues (Bourgis et al, 1999;Tan et al, 2010). These reports are in line with the phloem-specific expression of the Met Cycle genes and indicate that the reduction of AdoMet and SMM in the dep1 and mti1 mutants most likely represents a reduction of reduced S compounds in the phloem.…”

Improving Plant Nitrogen Use Efficiency through Alteration of Amino Acid Transport Processes

“…Within the seed, amino acids are taken up by the embryo for metabolism and the accumulation of storage compounds, such as proteins and starch (Lanfermeijer et al, 1990;Jenner et al, 1991;Hirner et al, 1998;Sanders et al, 2009;Zhang et al, 2015). Both loading of amino acids into the phloem and uptake into the embryo are key regulatory steps in N allocation from source to sink and require the activity of transport proteins (Schmidt et al, 2007;Tan et al, 2010;Zhang et al, 2010Zhang et al, , 2015Tegeder, 2014;Santiago and Tegeder, 2016). The function of these amino acid transporters impacts the number of pods and seeds that develop as well as the amount of seed storage compounds (Atkins et al, 1975;Hirel et al, 2007;Sanders et al, 2009;Tan et al, 2010;Zhang et al, 2015;Santiago and Tegeder, 2016).…”

“…Both loading of amino acids into the phloem and uptake into the embryo are key regulatory steps in N allocation from source to sink and require the activity of transport proteins (Schmidt et al, 2007;Tan et al, 2010;Zhang et al, 2010Zhang et al, , 2015Tegeder, 2014;Santiago and Tegeder, 2016). The function of these amino acid transporters impacts the number of pods and seeds that develop as well as the amount of seed storage compounds (Atkins et al, 1975;Hirel et al, 2007;Sanders et al, 2009;Tan et al, 2010;Zhang et al, 2015;Santiago and Tegeder, 2016). We hypothesized that these organic N transporters in source and sink also contribute to plant NUE and that their activities affect plant growth and development in N-poor as well as N-rich environments.…”

“…The uptake of N by the root is influenced by the availability of soil N and controlled by plant N assimilation processes and N metabolite levels as well as the N demand of the plant (Ruffel et al, 2011;Nacry et al, 2013;Stahl et al, 2016). In addition, recent work has resolved that amino acid transport processes in root and shoot strongly influence N uptake and metabolism, most probably through a feedback regulatory mechanism and shootto-root signaling (Miller et al, 2008;Sanders et al, 2009;Tan et al, 2010;Zhang et al, 2010Zhang et al, , 2015 Forde, 2014;Santiago and Tegeder, 2016). Nitrogen utilization efficiency (NUtE) is defined as total seed yield relative to total shoot N content (Moll et al, 1982) and is affected by several physiological factors, including N uptake, metabolism, allocation, and remobilization (Habash et al, 2001;Tsay et al, 2011;Girondé et al, 2015).…”

“…Nitrogen utilization efficiency (NUtE) is defined as total seed yield relative to total shoot N content (Moll et al, 1982) and is affected by several physiological factors, including N uptake, metabolism, allocation, and remobilization (Habash et al, 2001;Tsay et al, 2011;Girondé et al, 2015). In addition, regulated transport of N within the plant strongly influences the amount of N allocated to seeds and final seed yields (Rolletschek et al, 2005;Schmidt et al, 2007;Weigelt et al, 2008;Tan et al, 2010;Zhang et al, 2010Zhang et al, , 2015Carter and Tegeder, 2016;Santiago and Tegeder, 2016 Araus et al, 2016;Chen et al, 2017), nitrate allocation (Tsay et al, 2011), N metabolism (Ameziane et al, 2000Chichkova et al, 2001;Habash et al, 2001;Yamaya et al, 2002;Seiffert et al, 2004;Good et al, 2007;Shrawat et al, 2008;Peña et al, 2017), and its regulation (Yanagisawa et al, 2004). While generally successful, these studies often did not address the different components of NUE (i.e.…”