Difference in root K+ retention ability and reduced sensitivity of K+-permeable channels to reactive oxygen species confer differential salt tolerance in three Brassica species

被引:95
作者
Chakraborty, Koushik [1 ,2 ,3 ]
Bose, Jayakumar [2 ,3 ,4 ]
Shabala, Lana [2 ,3 ]
Shabala, Sergey [2 ,3 ]
机构
[1] ICAR Directorate Groundnut Res, Dept Plant Physiol, Junagadh 362001, Gujarat, India
[2] Univ Tasmania, Sch Land & Food, Private Bag 94, Hobart, Tas 7001, Australia
[3] Univ Tasmania, Tasmanian Inst Agr, Private Bag 94, Hobart, Tas 7001, Australia
[4] Univ Adelaide, Sch Agr Food & Wine, PMB1, Glen Osmond, SA 5064, Australia
基金
澳大利亚研究理事会;
关键词
H+-ATPase; ion homeostasis; membrane potential; potassium retention; ROS detoxification; sodium exclusion; tissue tolerance; NONSELECTIVE CATION CHANNELS; PLASMA-MEMBRANE CA2+; THALIANA CULTURED-CELLS; SALINITY TOLERANCE; STRESS TOLERANCE; H+-ATPASE; SIGNALING PATHWAYS; ARABIDOPSIS ROOTS; HYDROXYL RADICALS; OXIDATIVE STRESS;
D O I
10.1093/jxb/erw236
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
This work provides the mechanistic explanation for differential salt stress sensitivity amongst Brassica species and links it with regulation of root plasma membrane potential and the cytosolic K/Na ratio.Brassica species are known to possess significant inter and intraspecies variability in salinity stress tolerance, but the cell-specific mechanisms conferring this difference remain elusive. In this work, the role and relative contribution of several key plasma membrane transporters to salinity stress tolerance were evaluated in three Brassica species (B. napus, B. juncea, and B. oleracea) using a range of electrophysiological assays. Initial root growth assay and viability staining revealed that B. napus was most tolerant amongst the three species, followed by B. juncea and B. oleracea. At the mechanistic level, this difference was conferred by at least three complementary physiological mechanisms: (i) higher Na+ extrusion ability from roots resulting from increased expression and activity of plasma membrane SOS1-like Na+/H+ exchangers; (ii) better root K+ retention ability resulting from stress-inducible activation of H+-ATPase and ability to maintain more negative membrane potential under saline conditions; and (iii) reduced sensitivity of B. napus root K+-permeable channels to reactive oxygen species (ROS). The last two mechanisms played the dominant role and conferred most of the differential salt sensitivity between species. Brassica napus plants were also more efficient in preventing the stress-induced increase in GORK transcript levels and up-regulation of expression of AKT1, HAK5, and HKT1 transporter genes. Taken together, our data provide the mechanistic explanation for differential salt stress sensitivity amongst these species and shed light on transcriptional and post-translational regulation of key ion transport systems involved in the maintenance of the root plasma membrane potential and cytosolic K/Na ratio as a key attribute for salt tolerance in Brassica species.
引用
收藏
页码:4611 / 4625
页数:15
相关论文
共 83 条
[11]   Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley [J].
Bose, Jayakumar ;
Shabala, Lana ;
Pottosin, Igor ;
Zeng, Fanrong ;
Velarde-Buendia, Ana-Maria ;
Massart, Amandine ;
Poschenrieder, Charlotte ;
Hariadi, Yuda ;
Shabala, Sergey .
PLANT CELL AND ENVIRONMENT, 2014, 37 (03) :589-600
[12]   Calcium efflux systems in stress signaling and adaptation in plants [J].
Bose, Jayakumar ;
Pottosin, Igor I. ;
Shabala, Stanislav S. ;
Palmgren, Michael G. ;
Shabala, Sergey .
FRONTIERS IN PLANT SCIENCE, 2011, 2
[13]   Potassium as an intrinsic uncoupler of the plasma membrane H+-ATPase [J].
Buch-Pedersen, Morten J. ;
Rudashevskaya, Elena L. ;
Berner, Torben S. ;
Venema, Kees ;
Palmgren, Michael G. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2006, 281 (50) :38285-38292
[14]   Effects of different levels of soil salinity on yield attributes, accumulation of nitrogen, and micronutrients in Brassica spp. [J].
Chakraborty, K. ;
Sairam, R. K. ;
Bhaduri, D. .
JOURNAL OF PLANT NUTRITION, 2016, 39 (07) :1026-1037
[15]   Salinity-induced expression of pyrrolline-5-carboxylate synthetase determine salinity tolerance in Brassica spp [J].
Chakraborty, K. ;
Sairam, R. K. ;
Bhattacharya, R. C. .
ACTA PHYSIOLOGIAE PLANTARUM, 2012, 34 (05) :1935-1941
[16]   Evaluating relative contribution of osmotolerance and tissue tolerance mechanisms toward salinity stress tolerance in three Brassica species [J].
Chakraborty, Koushik ;
Bose, Jayakumar ;
Shabala, Lana ;
Eyles, Alieta ;
Shabala, Sergey .
PHYSIOLOGIA PLANTARUM, 2016, 158 (02) :135-151
[17]   Screening plants for salt tolerance by measuring K+ flux:: a case study for barley [J].
Chen, Z ;
Newman, I ;
Zhou, M ;
Mendham, N ;
Zhang, G ;
Shabala, S .
PLANT CELL AND ENVIRONMENT, 2005, 28 (10) :1230-1246
[18]   Combining ability of salinity tolerance on the basis of NaCl-induced K+ flux from roots of barley [J].
Chen, Zhonghua ;
Shabala, Sergey ;
Mendham, Neville ;
Newman, Ian ;
Zhang, Guoping ;
Zhou, Meixue .
CROP SCIENCE, 2008, 48 (04) :1382-1388
[19]   Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley [J].
Chen, Zhonghua ;
Pottosin, Igor I. ;
Cuin, Tracey A. ;
Fuglsang, Anja T. ;
Tester, Mark ;
Jha, Deepa ;
Zepeda-Jazo, Isaac ;
Zhou, Meixue ;
Palmgren, Michael G. ;
Newman, Ian A. ;
Shabala, Sergey .
PLANT PHYSIOLOGY, 2007, 145 (04) :1714-1725
[20]   Genetic behaviour of physiological traits conferring cytosolic K plus /?Na plus homeostasis in wheat [J].
Cuin, T. A. ;
Zhou, M. ;
Parsons, D. ;
Shabala, S. .
PLANT BIOLOGY, 2012, 14 (03) :438-446