Sulfate is transported at significant rates through the symbiosome membrane and is crucial for nitrogenase biosynthesis

被引:29
作者
Schneider, Sebastian [1 ]
Schintlmeister, Arno [2 ,3 ]
Becana, Manuel [4 ]
Wagner, Michael [2 ,3 ]
Woebken, Dagmar [2 ]
Wienkoop, Stefanie [1 ]
机构
[1] Univ Vienna, Dept Ecogen & Syst Biol, Div Mol Syst Biol, A-1090 Vienna, Austria
[2] Univ Vienna, Dept Microbiol & Ecosyst Sci, Div Microbial Ecol, Res Network Chem Meets Microbiol, Vienna, Austria
[3] Univ Vienna, Large Instrument Facil Adv Isotope Res, Vienna, Austria
[4] CSIC, Estn Expt Aula Dei, Zaragoza, Spain
基金
奥地利科学基金会;
关键词
legume nodules; nanoSIMS; nitrogen fixation; stable isotope labelling; sulfur deficiency; symbiotic sulfate transporter (SST1); PROTEOME ANALYSIS; SULFUR NUTRITION; GLOBAL CHANGES; PLANT-GROWTH; FIXATION; ASSIMILATION; GLUTATHIONE; METABOLISM; ROOTS; QUANTIFICATION;
D O I
10.1111/pce.13481
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Legume-rhizobia symbioses play a major role in food production for an ever growing human population. In this symbiosis, dinitrogen is reduced ("fixed") to ammonia by the rhizobial nitrogenase enzyme complex and is secreted to the plant host cells, whereas dicarboxylic acids derived from photosynthetically produced sucrose are transported into the symbiosomes and serve as respiratory substrates for the bacteroids. The symbiosome membrane contains high levels of SST1 protein, a sulfate transporter. Sulfate is an essential nutrient for all living organisms, but its importance for symbiotic nitrogen fixation and nodule metabolism has long been underestimated. Using chemical imaging, we demonstrate that the bacteroids take up 20-fold more sulfate than the nodule host cells. Furthermore, we show that nitrogenase biosynthesis relies on high levels of imported sulfate, making sulfur as essential as carbon for the regulation and functioning of symbiotic nitrogen fixation. Our findings thus establish the importance of sulfate and its active transport for the plant-microbe interaction that is most relevant for agriculture and soil fertility.
引用
收藏
页码:1180 / 1189
页数:10
相关论文
共 59 条
[1]   SULPHUR IN NITROGEN METABOLISM OF LEGUMES AND NON-LEGUMES [J].
ANDERSON, AJ ;
SPENCER, D .
AUSTRALIAN JOURNAL OF SCIENTIFIC RESEARCH SERIES B-BIOLOGICAL SCIENCES, 1950, 3 (04) :432-&
[2]   EFFECT OF SULFUR ON GROWTH, SULFUR AND NITROGEN CONCENTRATIONS, AND CRITICAL SULFUR CONCENTRATIONS OF SOME TROPICAL AND TEMPERATE PASTURE LEGUMES [J].
ANDREW, CS .
AUSTRALIAN JOURNAL OF AGRICULTURAL RESEARCH, 1977, 28 (05) :807-820
[3]   Sulfur Transport and Metabolism in Legume Root Nodules [J].
Becana, Manuel ;
Wienkoop, Stefanie ;
Matamoros, Manuel A. .
FRONTIERS IN PLANT SCIENCE, 2018, 9
[4]   CONTROLLING THE FALSE DISCOVERY RATE - A PRACTICAL AND POWERFUL APPROACH TO MULTIPLE TESTING [J].
BENJAMINI, Y ;
HOCHBERG, Y .
JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1995, 57 (01) :289-300
[5]  
BRADFORD MM, 1976, ANAL BIOCHEM, V72, P248, DOI 10.1016/0003-2697(76)90527-3
[6]   CONTROL OF LEGHAEMOGLOBIN SYNTHESIS IN SNAKE BEANS [J].
BROUGHTON, WJ ;
DILWORTH, MJ .
BIOCHEMICAL JOURNAL, 1971, 125 (04) :1075-+
[7]   Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport [J].
Buchner, P ;
Takahashi, H ;
Hawkesford, MJ .
JOURNAL OF EXPERIMENTAL BOTANY, 2004, 55 (404) :1765-1773
[8]   NITROGEN-FIXATION BY A RHIZOBIUM SP IN ASSOCIATION WITH NON-LEGUMINOUS PLANT-CELL CULTURES [J].
CHILD, JJ .
NATURE, 1975, 253 (5490) :350-351
[9]   Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus [J].
Colebatch, G ;
Desbrosses, G ;
Ott, T ;
Krusell, L ;
Montanari, O ;
Kloska, S ;
Kopka, J ;
Udvardi, MK .
PLANT JOURNAL, 2004, 39 (04) :487-512
[10]   Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays [J].
Colebatch, G ;
Kloska, S ;
Trevaskis, B ;
Freund, S ;
Altmann, T ;
Udvardi, MK .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2002, 15 (05) :411-420