Local and Systemic Metabolic Responses during Light-Induced Rapid Systemic Signaling

被引:47
作者
Choudhury, Feroza K. [1 ]
Devireddy, Amith R. [1 ,3 ,4 ]
Azad, Rajeev K. [1 ,2 ]
Shulaev, Vladimir [1 ]
Mittler, Ron [3 ,4 ]
机构
[1] Univ North Texas, Dept Biol Sci, Coll Arts & Sci, Denton, TX 76203 USA
[2] Univ North Texas, Dept Math, Denton, TX 76203 USA
[3] Univ Missouri, Coll Agr Food & Nat Resources, Sch Med, Div Plant Sci, Columbia, MO 65201 USA
[4] Univ Missouri, Dept Surg, Sch Med, Columbia, MO 65201 USA
基金
美国国家科学基金会;
关键词
REACTIVE OXYGEN; ANTIOXIDANT DEFENSE; HYDROGEN-PEROXIDE; OXIDATIVE STRESS; SINGLET OXYGEN; ACCLIMATION; ARABIDOPSIS; PHOTOSYNTHESIS; CALCIUM; ROS;
D O I
10.1104/pp.18.01031
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Plants evolved multiple signaling pathways that transduce light-related signals between leaves. These are thought to improve light stress acclimation in a process termed systemic acquired acclimation. Although responses to light stress have been studied extensively in local leaves, and to a lesser degree in systemic leaves, little is known about the responses that occur in the different tissues that connect the local to the systemic leaves. These could be important in defining the specificity of the systemic response as well as in supporting the generation of different systemic signals. Here, we report that local application of light stress to one rosette leaf of bolting Arabidopsis (Arabidopsis thaliana) plants resulted in a metabolic response that encompassed local, systemic and transport tissues (stem tissues that connect the local to the systemic tissues), demonstrating a high degree of physical and metabolic continuity between different tissues throughout the plant. Our results further indicate that the response of many of the systemically altered metabolites is associated with the function of the reactive oxygen species wave and that the levels of eight different metabolites are altered in a similar manner in all tissues tested (local, systemic, and transport). These compounds could define a core metabolic signature for light stress that propagates from the local to the systemic leaves. Our findings suggest that metabolic changes occurring in cells that connect the local and systemic tissues play an important role in systemic acquired acclimation and could convey specificity to the rapid systemic response of plants to light stress.
引用
收藏
页码:1461 / 1472
页数:12
相关论文
共 57 条
[1]   Alternative electron transport pathways in photosynthesis: a confluence of regulation [J].
Alric, Jean ;
Johnson, Xenie .
CURRENT OPINION IN PLANT BIOLOGY, 2017, 37 :78-86
[2]   Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis [J].
Bode, Rainer ;
Ivanov, Alexander G. ;
Huner, Norman P. A. .
PHOTOSYNTHESIS RESEARCH, 2016, 128 (03) :287-312
[3]   Uncoupling High Light Responses from Singlet Oxygen Retrograde Signaling and Spatial-Temporal Systemic Acquired Acclimation [J].
Carmody, Melanie ;
Crisp, Peter A. ;
d'Alessandro, Stefano ;
Ganguly, Diep ;
Gordon, Matthew ;
Havaux, Michel ;
Albrecht-Borth, Veronica ;
Pogson, Barry J. .
PLANT PHYSIOLOGY, 2016, 171 (03) :1734-1749
[4]   Changes in the Phosphoproteome and Metabolome Link Early Signaling Events to Rearrangement of Photosynthesis and Central Metabolism in Salinity and Oxidative Stress Response in Arabidopsis [J].
Chen, Yanmei ;
Hoehenwarter, Wolfgang .
PLANT PHYSIOLOGY, 2015, 169 (04) :3021-3033
[5]   Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals [J].
Choi, Won-Gyu ;
Miller, Gad ;
Wallace, Ian ;
Harper, Jeffrey ;
Mittler, Ron ;
Gilroy, Simon .
PLANT JOURNAL, 2017, 90 (04) :698-707
[6]   Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants [J].
Choi, Won-Gyu ;
Toyota, Masatsugu ;
Kim, Su-Hwa ;
Hilleary, Richard ;
Gilroy, Simon .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (17) :6497-6502
[7]   Hydraulic signals in long-distance signaling [J].
Christmann, Alexander ;
Grill, Erwin ;
Huang, Jin .
CURRENT OPINION IN PLANT BIOLOGY, 2013, 16 (03) :293-300
[8]   PsbS is required for systemic acquired acclimation and post-excess-light-stress optimization of chlorophyll fluorescence decay times in Arabidopsis [J].
Ciszak, Kamil ;
Kulasek, Milena ;
Barczak, Anna ;
Grzelak, Justyna ;
Mackowski, Sebastian ;
Karpinsk, Stanislaw .
PLANT SIGNALING & BEHAVIOR, 2015, 10 (01) :e982018-1
[9]   Rapid Recovery Gene Downregulation during Excess-Light Stress and Recovery in Arabidopsis [J].
Crisp, Peter A. ;
Ganguly, Diep R. ;
Smith, Aaron B. ;
Murray, Kevin D. ;
Estavillo, Gonzalo M. ;
Searle, Iain ;
Ford, Ethan ;
Bogdanovic, Ozren ;
Lister, Ryan ;
Borevitz, Justin O. ;
Eichten, Steven R. ;
Pogson, Barry J. .
PLANT CELL, 2017, 29 (08) :1836-1863
[10]   Overexpression of Glycolate Oxidase Confers Improved Photosynthesis under High Light and High Temperature in Rice [J].
Cui, Li-Li ;
Lu, Yu-sheng ;
Li, Yong ;
Yang, Chengwei ;
Peng, Xin-Xiang .
FRONTIERS IN PLANT SCIENCE, 2016, 7