Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids

Plant Journal

Volumn 81, Issue 1, 2015, Pages 134-146

  Zhang, Lizhi ^a,c   Garneau, Matthew G ^a   Majumdar, Rajtilak ^a,d   Grant, Jan ^b   Tegeder, Mechthild ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^c OHIO STATE UNIVERSITY   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

biomass production; nitrogen and carbon metabolism; phloem and seed loading; seed yield; sink development; source to sink amino acid transport

Indexed keywords

AMINO ACIDS; BIOMASS; CELL MEMBRANES; METABOLISM; NITROGEN; PHYSIOLOGY; PLANTS (BOTANY); PROTEINS; SEED;

AMINO ACID TRANSPORT; BIOMASS PRODUCTIONS; CARBON METABOLISM; SEED YIELD; SINK DEVELOPMENT;

LOADING;

PISUM SATIVUM;

AMINO ACID; CARBON; NITROGEN; VEGETABLE PROTEIN;

BIOMASS; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PEA; PHLOEM; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; PLANT SEED; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACIDS; BIOLOGICAL TRANSPORT; BIOMASS; CARBON; FRUIT; GENE EXPRESSION REGULATION, PLANT; NITROGEN; PEAS; PHLOEM; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SEEDS;

EID: 84920271390     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12716     Document Type: Article

References (84)

1. Aoyama, C., Santa, T., Tsunoda, M., Fukushima, T., Kitada, C., and, Imai, K., (2004) A fully automated amino acid analyzer using NBD-F as a fluorescent derivatization reagent. Biomed. Chromatogr. 18, 630-636.
2. Atkins, C.A., (2000) Biochemical aspects of assimilate transfers along the phloem path: N-solutes in lupins. Aust. J. Plant Physiol. 27, 531-537.
3. Atkins, C.A., and, Beevers, L., (1990) Synthesis, transport and utilization of translocated solutes of nitrogen. In Nitrogen in Higher Plants (, Abrol, Y.P., ed.). Somerset: Research Studies Press, pp. 223-295.
4. Atkins, C.A., and, Smith, P.M., (2007) Translocation in legumes: assimilates, nutrients, and signaling molecules. Plant Physiol. 144, 550-561.
5. Ayre, B.G., (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol. Plant, 4, 377-394.
6. Bauer, A., Joy, K.W., and, Urquhart, A.A., (1977) Amino acid metabolism of pea leaves: labeling studies on utilization of amides. Plant Physiol. 59, 920-924.
7. Borisjuk, L., Rolletschek, H., Wobus, U., and, Weber, H., (2003) Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds. J. Exp. Bot. 54, 503-512.
8. Brady, S.M., Orlando, D.A., Lee, J.Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U., and, Benfey, P.N., (2007) A High-resolution root spatiotemporal map reveals dominant expression patterns. Science, 318, 801-806.
9. Braun, D.M., Wang, L., and, Ruan, Y.-L., (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. J. Exp. Bot. 65, 1713-1735.
10. Chen, M.H., Liu, L.F., Chen, Y.R., Wu, H.K., and, Yu, S.M., (1994) Expression of α-amylases, carbohydrate metabolism, and autophagy in cultured rice cells are coordinately regulated by sugar nutrient. Plant J. 6, 625-636.
11. Corbesier, L., Bernier, G., and, Perilleux, C., (2002) C:N ratio increases in the phloem sap during floral transition of the long-day plants Sinapis alba and Arabidopsis thaliana. Plant Cell Physiol. 43, 684-688.
12. Crawford, N.M., (1995) Nitrate: nutrient and signal for plant growth. Plant Cell, 7, 859-868.
13. De Jong, A., and, Borstlap, A.C., (2000) Transport of amino acids (L-valine, L-lysine, L-glutamic acid) and sucrose into plasma membrane vesicles isolated from cotyledons of developing pea seeds. J. Exp. Bot. 51, 1663-1670.
14. De Jong, A., and, Wolswinkel, P., (1995) Differences in release of endogenous sugars and amino acids from attached and detached seed coats of developing pea seeds. Physiol. Plant., 94, 78-86.
15. De Jong, A., Koerselman-Kooij, J.W., Schuurmans, J.A.M.J., and, Borstlap, A.C., (1997) The mechanism of amino acid efflux from seed coats of developing pea seeds as revealed by uptake experiments. Plant Physiol. 114, 731-736.
16. Egli, D.B., (2005) Flowering, pod set, and reproductive success in soya bean. J. Agron. Crop Sci. 191, 283-291.
17. Egli, D.B., (2010) SOYPOD: a model of fruit set in soybean. Agron. J. 102, 39-47.
18. Fischer, W.N., Kwart, M., Hummel, S., and, Frommer, W.B., (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol. Chem. 270, 16315-16320.
19. +-cotransporters for cellular import of neutral and charged amino acids. Plant J. 29, 717-731.
20. Gaufichon, L., Reisdorf-Cren, M., Rothstein, S.J., Chardon, F., and, Suzuki, A., (2010) Biological functions of asparagine synthetase in plants. Plant Sci. 179, 141-15310.
21. Gibson, S. I., (2005) Control of plant development and gene expression by sugar signaling. Curr. Opin. Plant Biol. 8, 93-102.
22. Grant, J.E., Cooper, P.A., McAra, A.E., and, Frew, T.J., (1995) Transformation of peas (Pisum sativum L.) using immature cotyledons. Plant Cell Rep. 15, 254-258.
23. Gutiérrez, R.A., Stokes, T.L., Thum, K., et al. (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc. Natl Acad. Sci. USA, 105, 4939-4944.
24. Hajdukiewicz, P., Svab, Z., and, Maliga, P., (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989-994.
25. Hammes, U.Z., Nielsen, E., Honaas, L.A., Taylor, C.G., and, Schachtman, D.P., (2006) AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J. 48, 414-426.
26. Hirner, B., Fischer, W.N., Rentsch, D., Kwart, M., and, Frommer, W.B., (1998) Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. Plant J. 14, 535-544.
27. Ladwig, F., Stahl, M., Ludewig, U., Hirner, A.A., Hammes, U.Z., Stadler, R., Harter, K., and, Koch, W., (2012) Siliques Are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol. 158, 1643-1655.
28. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W.B., and, Patrick, J.W., (2003) Phloem loading and unloading of amino acids and sugars. Plant, Cell Environ. 26, 37-56.
29. Lam, H.M., Hsieh, M.H., and, Coruzzi, G., (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J. 16, 345-353.
30. Lanfermeijer, F.C., Koerselman-kooij, J., and, Borstlap, A.C., (1990) Changing kinetics of L-valine uptake by immature pea cotyledons during development. Planta, 181, 576-582.
31. Lanfermeijer, F.C., Van Oene, M.A., and, Borstlap, A.C., (1992) Compartmental analysis of amino acid release from attached and detached pea seed coats. Planta, 187, 75-82.
32. Lawlor, D.W., (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J. Exp. Bot. 53, 773-787.
33. Livak, K.J., and, Schmittgen, T.D., (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-Δ Δ C T. Methods, 25, 402-408.
34. Ma, Q., Longnecker, N., and, Atkins, C.A., (1998) Exogenous cytokinin and nitrogen do not increase grain yield in narrow-leafed lupin. Crop Sci. 38, 717-721.
35. McPhee, K.E., Gollasch, S., Schroeder, H.E., and, Higgins, T.J.V., (2004) Gene technology in pea. In Transgenic Crops of the World-Essential Protocols (, Curtis, I.S., ed.). Dordrecht: Kluwer Academic Publishers, pp. 351-359.
36. Miller, A.J., Shen, Q., and, Xu, G., (2009) Freeways in the plant: transporters for N, P and S and their regulation. Curr. Opin. Plant Biol. 12, 284-290.
37. Miranda, M., Borisjuk, L., Tewes, A., Heim, U., Sauer, N., Wobus, U., and, Weber, H., (2001) Amino acid permeases in developing seeds of Vicia faba L.: expression precedes storage protein synthesis and is regulated by amino acid supply. Plant J. 28, 61-71.
38. Miranda, M., Borisjuk, L., Tewes, A., Dietrich, D., Rentsch, D., Weber, H., and, Wobus, U., (2003) Peptide and amino acid transporters are differentially regulated during seed development and germination in faba bean. Plant Physiol. 132, 1950-1960.
39. Mita, S., Suzuki-Fujii, K., and, Nakamura, K., (1995) Sugar-inducible expression of a gene for β-amylase in Arabidopsis thaliana. Plant Physiol. 107, 895-904.
40. Oaks, A., (1992) A re-evaluation of nitrogen assimilation in roots. Bioscience, 42, 105-111.
41. Offler, C.E., McCurdy, D.W., Patrick, J.W., and, Talbot, M.J., (2003) Transfer cells: cells specialized for a special purpose. Ann. Rev. Plant Biol. 54, 431-454.
42. Pate, J.S., (1980) Transport and partitioning of nitrogenous solutes. Ann. Rev. Plant Physiol. 31, 313-340.
43. Pate, J.S., and, Atkins, C.A., (1983) Xylem and phloem transport and the functional economy of carbon and nitrogen of a legume leaf. Plant Physiol. 71, 835-840.
44. Patrick, J.W., (1997) Phloem unloading: sieve element unloading and post-sieve element transport. Ann. Rev. Plant Physiol. 48, 191-222.
45. Patrick, J.W., Offler, C.E., and, van Bel, A.J.E., (2003) Seed development: nutrient loading of seeds. In Encyclopedia of Applied Plant Sciences (, Thomas, B., Murphy, D., and, Murray, B., eds). London, UK: Academic Press, pp. 1240-1250.
46. Paul, M.J., and, Pellny, T.K., (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J. Exp. Bot. 54, 539-547.
47. Pélissier, H.C., and, Tegeder, M., (2007) PvUPS1 plays a role in source-sink transport of allantoin in French bean (Phaseolus vulgaris). Funct. Plant Biol. 34, 282-291.
48. Price, J., Laxmi, A., St Martin, S.K., and, Jang, J.C., (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell, 16, 2128-2150.
49. Rentsch, D., Schmidt, S., and, Tegeder, M., (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett. 581, 2281-2289.
50. Reynolds, S.J., and, Smith, S.M., (1995) Regulation of expression of the cucumber isocitrate lyase gene in cotyledons upon seed germination and by sucrose. Plant Mol. Biol. 29, 885-896.
51. Reynolds, M., Foulkes, M.J., Slafer, G.A., Berry, P., Parry, M.A.J., Snape, J.W., and, Angus, W.J., (2009) Raising yield potential in wheat. J. Exp. Bot. 60, 1899-1918.
52. Rolletschek, H., Hosein, F., Miranda, M., Heim, U., Gotz, K.P., Schlereth, A., Borisjuk, L., Saalbach, I., Wobus, U., and, Weber, H., (2005) Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol. 137, 1236-1249.
53. Ruffel, S., Krouk, G., and, Coruzzi, G.M., (2010) A systems view of responses to nutritional cues in Arabidopsis: toward a paradigm shift for predictive network modeling. Plant Physiol. 152, 445-452.
54. Sanders, A., Collier, R., Trethewy, A., Gould, G., Sieker, R., and, Tegeder, M., (2009) AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J. 59, 540-552.
55. Scheible, W.R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., Schindelasch, D., Thimm, O., Udvardi, M.K., and, Stitt, M., (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136, 2483-2499.
56. Schmidt, R., Stransky, H., and, Koch, W., (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta, 226, 805-813.
57. Schroeder, H.E., Schotz, A.H., Wardley-Richardson, T., Spencer, D., and, Higgins, T.J.V., (1993) Transformation and regeneration of two cultivars of pea. Plant Physiol. 101, 751-757.
58. Sheen, J., (1994) Feedback control of gene expression. Photosyn. Res. 39, 427-438.
59. Silvente, S., Reddy, P.M., Khandual, S., Blanco, L., Alvarado-Affantranger, X., Sanchez, F., and, Lara-Flores, M., (2008) Evidence for sugar signalling in the regulation of asparagine synthetase gene expressed in Phaseolus vulgaris roots and nodules. J. Exp. Bot. 59, 1279-1294.
60. Smeekens, S., (2000) Sugar-induced signal transduction in plants. Ann. Rev. Plant Physiol. Mol. Biol. 51, 49-81.
61. Smidansky, E.D., Martin, J.M., Hannah, L.C., Fischer, A.M., and, Giroux, M.J., (2003) Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta, 216, 656-664.
62. Tan, Q., Grennan, A.K., Pélissier, H.C., Rentsch, D., and, Tegeder, M., (2008) Characterization and expression of French bean amino acid transporter PvAAP1. Plant Sci. 174, 348-356.
63. Tan, Q., Zhang, L., Grant, J., Cooper, P., and, Tegeder, M., (2010) Altered phloem transport of S-methylmethionine affects plant metabolism and seed number in pea plants. Plant Physiol. 154, 1886-1896.
64. Tegeder, M., (2012) Transporters for amino acids in plant cells: some functions and many unknowns. Curr. Opin. Plant Biol. 15, 315-321.
65. Tegeder, M., (2014) Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J. Exp. Bot. 65, 1865-1878.
66. Tegeder, M., and, Rentsch, D., (2010) Uptake and partitioning of amino acids and peptides. Mol. Plant, 3, 997-1011.
67. Tegeder, M., and, Ward, J.M., (2012) Molecular evolution of plant AAP and LHT amino acid transporters. Front. Plant Physiol. 3, 1-11.
68. Tegeder, M., Wang, X.D., Frommer, W.B., Offler, C.E., and, Patrick, J.W., (1999) Sucrose transport into developing seeds of Pisum sativum L. Plant J. 18, 151-161.
69. Tegeder, M., Offler, C.E., Frommer, W.B., and, Patrick, J.W., (2000a) Amino acid transporters are localized to transfer cells of developing pea seeds. Plant Physiol. 122, 319-325.
70. Tegeder, M., Thomas, M., Hetherington, L., Wang, X.D., Offler, C.E., and, Patrick, J.W., (2000b) Genotypic differences in seed growth rates of Phaseolus vulgaris L. II. Factors contributing to cotyledon sink activity and sink size. Aust. J. Plant Physiol. 27, 119-128.
71. Tegeder, M., Tan, Q., Grennan, A.K., and, Patrick, J.W., (2007) Amino acid transporter expression and localisation studies in pea (Pisum sativum). Funct. Plant Biol. 34, 1019-1028.
72. Tegeder, M., Rentsch, D., and, Patrick, J.W., (2011) Organic carbon and nitrogen transporters. In Plant Plasma Membrane: Plant Cell Monographs (, Murphy, A., Peer, W., and, Schulz, B., eds). Berlin: Springer, pp. 331-352.
73. Tegeder, M., Ruan, Y.L., and, Patrick, J.W., (2013) Roles of membrane transporters in phloem functions. In Biochemistry of Phloem (, Thompson, G., and, Van Bel, A., eds). Oxford: Wiley-Blackwell, pp. 63-101.
74. Thum, K., Shin, M., Gutierrez, R., Mukherjee, I., Katari, M., Nero, D., Shasha, D., and, Coruzzi, G., (2008) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst. Biol. 2, 31.
75. Urquhart, A.A., and, Joy, K.W., (1981) Use of phloem exudate technique in the study of amino acid transport in pea plants. Plant Physiol. 68, 750-754.
76. Urquhart, A.A., and, Joy, K.W., (1982) Transport, metabolism, and redistribution of Xylem-borne amino acids in developing pea shoots. Plant Physiol. 69, 1226-1232.
77. Van Bel, A.J.E., (1990) Xylem-phloem exchange via the rays: the undervalued route of transport. J. Exp. Bot. 41, 631-644.
78. Walch-Liu, P., Filleur, S., Gan, Y., and, Forde, B.G., (2005) Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply. Photosyn. Res. 83, 239-250.
79. Weber, H., Borisjuk, L., and, Wobus, U., (2005) Molecular physiology of legume seed development. Annu. Rev. Plant Biol. 56, 253-279.
80. Weigelt, K., Küster, H., Radchuk, R., Müller, M., Weichert, H., Fait, A., Fernie, A.R., Saalbach, I., and, Weber, H., (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism and highlights the importance of mitochondrial metabolism. Plant J. 55, 909-926.
81. Wimmers, L.E., and, Turgeon, R., (1991) Transfer cells and solute uptake in minor veins of Pisum sativum leaves. Planta, 186, 2-12.
82. Wingenter, K., Schulz, A., Wormit, A., Wic, S., Trentmann, O., Hoermiller, I.I., Heyer, A.G., Marten, I., Hedrich, R., and, Neuhaus, H.E., (2010) Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signaling, and seed yield in Arabidopsis. Plant Physiol. 154, 665-677.
83. Wong, H.K., Chan, H.K., and, Coruzzi, G.M., Lam, H.M., (2004) Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis. Plant Physiol. 134, 332-338.
84. Zhang, L., Tan, Q., Lee, R., Trethewy, A., Lee, Y.H., and, Tegeder, M., (2010) Altered xylem-phloem transfer of amino acids affects metabolism and leads to increased seed yield and oil content in Arabidopsis. Plant Cell, 22, 3603-3620.