Two NHX‐type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress
Abstract
Summary The NHX‐type cation/H + transporters in plants have been shown to mediate Na + (K + )/H + exchange for salinity tolerance and K + homoeostasis. In this study, we identified and characterized two NHX homologues, HtNHX1 and HtNHX2 from an infertile and salinity tolerant species Helianthus tuberosus (cv. Nanyu No. 1). HtNHX1 and HtNHX2 share identical 5′‐ and 3′‐UTR and coding regions, except for a 342‐bp segment encoding 114 amino acids (L 272 to Q 385 ) which is absent in HtNHX2 . Both hydroponics and soil culture experiments showed that the expression of HtNHX1 or HtNHX2 improved the rice tolerance to salinity. Expression of HtNHX2 , but not HtNHX1 , increased rice grain yield, harvest index, total nutrient uptake under K + ‐limited salt‐stress or general nutrient deficiency conditions. The results provide a novel insight into NHX function in plant mineral nutrition.
- Authors:
-
- State Key Laboratory of Crop Genetics and Germplasm Enhancement Nanjing Agricultural University Nanjing China, Key Laboratory of Plant Nutrition and Fertilization in Low‐Middle Reaches of the Yangtze River Ministry of Agriculture Nanjing Agricultural University Nanjing China
- Key Laboratory of Plant Nutrition and Fertilization in Low‐Middle Reaches of the Yangtze River Ministry of Agriculture Nanjing Agricultural University Nanjing China
- Department of Plant Sciences University of California Davis CA USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1393988
- Alternate Identifier(s):
- OSTI ID: 1393989
- Resource Type:
- Published Article
- Journal Name:
- Plant Biotechnology Journal
- Additional Journal Information:
- Journal Name: Plant Biotechnology Journal Journal Volume: 16 Journal Issue: 1; Journal ID: ISSN 1467-7644
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Zeng, Yang, Li, Qing, Wang, Haiya, Zhang, Jianliang, Du, Jia, Feng, Huimin, Blumwald, Eduardo, Yu, Ling, and Xu, Guohua. Two NHX‐type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress. United Kingdom: N. p., 2017.
Web. doi:10.1111/pbi.12773.
Zeng, Yang, Li, Qing, Wang, Haiya, Zhang, Jianliang, Du, Jia, Feng, Huimin, Blumwald, Eduardo, Yu, Ling, & Xu, Guohua. Two NHX‐type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress. United Kingdom. https://doi.org/10.1111/pbi.12773
Zeng, Yang, Li, Qing, Wang, Haiya, Zhang, Jianliang, Du, Jia, Feng, Huimin, Blumwald, Eduardo, Yu, Ling, and Xu, Guohua. Thu .
"Two NHX‐type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress". United Kingdom. https://doi.org/10.1111/pbi.12773.
@article{osti_1393988,
title = {Two NHX‐type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress},
author = {Zeng, Yang and Li, Qing and Wang, Haiya and Zhang, Jianliang and Du, Jia and Feng, Huimin and Blumwald, Eduardo and Yu, Ling and Xu, Guohua},
abstractNote = {Summary The NHX‐type cation/H + transporters in plants have been shown to mediate Na + (K + )/H + exchange for salinity tolerance and K + homoeostasis. In this study, we identified and characterized two NHX homologues, HtNHX1 and HtNHX2 from an infertile and salinity tolerant species Helianthus tuberosus (cv. Nanyu No. 1). HtNHX1 and HtNHX2 share identical 5′‐ and 3′‐UTR and coding regions, except for a 342‐bp segment encoding 114 amino acids (L 272 to Q 385 ) which is absent in HtNHX2 . Both hydroponics and soil culture experiments showed that the expression of HtNHX1 or HtNHX2 improved the rice tolerance to salinity. Expression of HtNHX2 , but not HtNHX1 , increased rice grain yield, harvest index, total nutrient uptake under K + ‐limited salt‐stress or general nutrient deficiency conditions. The results provide a novel insight into NHX function in plant mineral nutrition.},
doi = {10.1111/pbi.12773},
journal = {Plant Biotechnology Journal},
number = 1,
volume = 16,
place = {United Kingdom},
year = {Thu Sep 21 00:00:00 EDT 2017},
month = {Thu Sep 21 00:00:00 EDT 2017}
}
https://doi.org/10.1111/pbi.12773
Web of Science
Works referenced in this record:
Salt Tolerance Conferred by Overexpression of a Vacuolar Na+/H+ Antiport in Arabidopsis
journal, August 1999
- Apse, M. P.
- Science, Vol. 285, Issue 5431
Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake
journal, April 2014
- Andres, Z.; Perez-Hormaeche, J.; Leidi, E. O.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
Correlations in concentrations, xylem and phloem flows, and partitioning of elements and ions in intact plants. A summary and statistical re-evaluation of modelling experiments in Ricinus communis
journal, December 2009
- Peuke, Andreas D.
- Journal of Experimental Botany, Vol. 61, Issue 3
The Na+/H+ exchanger Nhx1p regulates the initiation of Saccharomyces cerevisiae vacuole fusion
journal, September 2010
- Qiu, Q. -S.; Fratti, R. A.
- Journal of Cell Science, Vol. 123, Issue 19
Rapid increase of vacuolar volume in response to salt stress
journal, January 2003
- Mimura, Tetsuro; Kura-Hotta, Mariko; Tsujimura, Tomoko
- Planta, Vol. 216, Issue 3
Salinity tolerance of crops - what is the cost?
journal, June 2015
- Munns, Rana; Gilliham, Matthew
- New Phytologist, Vol. 208, Issue 3
Adaptation of potassium translocation into the shoot of maize (Zea mays) to shoot demand: Evidence for xylem loading as a regulating step
journal, October 1992
- Engels, Christof; Marschner, Horst
- Physiologia Plantarum, Vol. 86, Issue 2
Improving phosphorus use efficiency: a complex trait with emerging opportunities
journal, February 2017
- Heuer, Sigrid; Gaxiola, Roberto; Schilling, Rhiannon
- The Plant Journal, Vol. 90, Issue 5
A Novel Plant Vacuolar Na + /H + Antiporter Gene Evolved by DNA Shuffling Confers Improved Salt Tolerance in Yeast
journal, May 2010
- Xu, Kai; Zhang, Hui; Blumwald, Eduardo
- Journal of Biological Chemistry, Vol. 285, Issue 30
On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils
journal, October 2015
- Shabala, Sergey; Bose, Jayakumar; Fuglsang, Anja Thoe
- Journal of Experimental Botany, Vol. 67, Issue 4
Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit
journal, August 2001
- Zhang, Hong-Xia; Blumwald, Eduardo
- Nature Biotechnology, Vol. 19, Issue 8
Dynamic Aspects of Ion Accumulation by Vesicle Traffic Under Salt Stress in Arabidopsis
journal, September 2009
- Hamaji, Kohei; Nagira, Megumi; Yoshida, Katsuhisa
- Plant and Cell Physiology, Vol. 50, Issue 12
Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump
journal, September 2001
- Gaxiola, R. A.; Li, J.; Undurraga, S.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
Genomic structure and differential expression of two tandem-arranged GSTZ genes in rice
journal, June 2004
- Tsuchiya, Tokuji; Takesawa, Toshikazu; Kanzaki, Hiroyuki
- Gene, Vol. 335
The Arabidopsis Intracellular Na + /H + Antiporters NHX5 and NHX6 Are Endosome Associated and Necessary for Plant Growth and Development
journal, January 2011
- Bassil, Elias; Ohto, Masa-aki; Esumi, Tomoya
- The Plant Cell, Vol. 23, Issue 1
Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity
journal, October 2003
- Yamaguchi, T.; Apse, M. P.; Shi, H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 21
Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation
journal, March 2009
- Ai, Penghui; Sun, Shubin; Zhao, Jianning
- The Plant Journal, Vol. 57, Issue 5
Potassium activities in cell compartments of salt-grown barley leaves
journal, February 2003
- Cuin, T. A.
- Journal of Experimental Botany, Vol. 54, Issue 383
Regulation of K + Uptake and Transport to the Xylem in Barley Roots; K + Distribution Determined by Electron Probe X-ray Microanalysis of Frozen-Hydrated Cells
journal, January 1990
- Drew, M. C.; Webb, J.; Saker, L. R.
- Journal of Experimental Botany, Vol. 41, Issue 7
Plant salt-tolerance mechanisms
journal, June 2014
- Deinlein, Ulrich; Stephan, Aaron B.; Horie, Tomoaki
- Trends in Plant Science, Vol. 19, Issue 6
Uptake and long-distance transport of phosphate, potassium and chloride in relation to internal ion concentrations in barley: evidence of non-allosteric regulation
journal, May 1984
- Drew, M. C.; Saker, L. R.
- Planta, Vol. 160, Issue 6
Economically Viable Components from Jerusalem Artichoke (Helianthus tuberosus L.) in a Biorefinery Concept
journal, April 2015
- Johansson, Eva; Prade, Thomas; Angelidaki, Irini
- International Journal of Molecular Sciences, Vol. 16, Issue 12
Ion Exchangers NHX1 and NHX2 Mediate Active Potassium Uptake into Vacuoles to Regulate Cell Turgor and Stomatal Function in Arabidopsis
journal, March 2012
- Barragán, Verónica; Leidi, Eduardo O.; Andrés, Zaida
- The Plant Cell, Vol. 24, Issue 3
Vacuolar Na+/H+ NHX-Type Antiporters Are Required for Cellular K+ Homeostasis, Microtubule Organization and Directional Root Growth
journal, August 2014
- McCubbin, Tyler; Bassil, Elias; Zhang, Shiqi
- Plants, Vol. 3, Issue 3
Protection of Plasma Membrane K + Transport by the Salt Overly Sensitive1 Na + -H + Antiporter during Salinity Stress
journal, September 2004
- Qi, Zhi; Spalding, Edgar P.
- Plant Physiology, Vol. 136, Issue 1
A Novel Intracellular K + /H + Antiporter Related to Na + /H + Antiporters Is Important for K + Ion Homeostasis in Plants
journal, April 2003
- Venema, Kees; Belver, Andrés; Marín-Manzano, M. Carmen
- Journal of Biological Chemistry, Vol. 278, Issue 25
Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes
journal, October 2010
- Fukuda, Atsunori; Nakamura, Atsuko; Hara, Naho
- Planta, Vol. 233, Issue 1
Tuning plant signaling and growth to survive salt
journal, September 2015
- Julkowska, Magdalena M.; Testerink, Christa
- Trends in Plant Science, Vol. 20, Issue 9
Sterols and sphingolipids differentially function in trafficking of the Arabidopsis ABCB19 auxin transporter
journal, February 2013
- Yang, Haibing; Richter, Gregory L.; Wang, Xia
- The Plant Journal, Vol. 74, Issue 1
Knockdown of a Rice Stelar Nitrate Transporter Alters Long-Distance Translocation But Not Root Influx
journal, October 2012
- Tang, Zhong; Fan, Xiaorong; Li, Qing
- Plant Physiology, Vol. 160, Issue 4
Na + /H + Antiport in Isolated Tonoplast Vesicles from Storage Tissue of Beta vulgaris
journal, May 1985
- Blumwald, Eduardo; Poole, Ronald J.
- Plant Physiology, Vol. 78, Issue 1
Transpiration, Potassium Uptake and Flow in Tobacco as Affected by Nitrogen Forms and Nutrient Levels
journal, March 2005
- Lu, Y. X.; Li, C. J.; Zhang, F. S.
- Annals of Botany, Vol. 95, Issue 6
The Role of a Potassium Transporter OsHAK5 in Potassium Acquisition and Transport from Roots to Shoots in Rice at Low Potassium Supply Levels
journal, August 2014
- Yang, T.; Zhang, S.; Hu, Y.
- PLANT PHYSIOLOGY, Vol. 166, Issue 2
The Arabidopsis Na + /H + Antiporters NHX1 and NHX2 Control Vacuolar pH and K + Homeostasis to Regulate Growth, Flower Development, and Reproduction
journal, September 2011
- Bassil, Elias; Tajima, Hiromi; Liang, Yin-Chih
- The Plant Cell, Vol. 23, Issue 9
Conserved and Diversified Gene Families of Monovalent Cation/H+ Antiporters from Algae to Flowering Plants
journal, January 2012
- Chanroj, Salil; Wang, Guoying; Venema, Kees
- Frontiers in Plant Science, Vol. 3
Vacuolar cation/H + exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1 , the Arabidopsis vacuolar Na + /H + antiporter
journal, October 2003
- Apse, Maris P.; Sottosanto, Jordan B.; Blumwald, Eduardo
- The Plant Journal, Vol. 36, Issue 2
Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR
journal, September 1995
- Liu, Yao-Guang; Mitsukawa, Norihiro; Oosumi, Teruko
- The Plant Journal, Vol. 8, Issue 3
The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato
journal, February 2010
- Leidi, Eduardo O.; Barragán, Verónica; Rubio, Lourdes
- The Plant Journal, Vol. 61, Issue 3
HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants
journal, December 2009
- Horie, Tomoaki; Hauser, Felix; Schroeder, Julian I.
- Trends in Plant Science, Vol. 14, Issue 12
Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response
journal, June 2002
- Yokoi, Shuji; Quintero, Francisco J.; Cubero, Beatriz
- The Plant Journal, Vol. 30, Issue 5
Effect of NO−3 -N Enrichment on Seawater Stress Tolerance of Jerusalem Artichoke (Helianthus tuberosus)
journal, February 2008
- Long, Xiao-Hua; Mehta, S. K.; Liu, Zhao-Pu
- Pedosphere, Vol. 18, Issue 1
Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium
journal, January 2004
- Volkov, V.; Wang, B.; Dominy, P. J.
- Plant, Cell and Environment, Vol. 27, Issue 1
Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development
journal, September 2012
- Bassil, E.; Coku, A.; Blumwald, E.
- Journal of Experimental Botany, Vol. 63, Issue 16
Plant Nitrogen Assimilation and Use Efficiency
journal, June 2012
- Xu, Guohua; Fan, Xiaorong; Miller, Anthony J.
- Annual Review of Plant Biology, Vol. 63, Issue 1
How do vacuolar NHX exchangers function in plant salt tolerance?
journal, July 2010
- Jiang, Xingyu; Leidi, Eduardo O.; Pardo, Jose M.
- Plant Signaling & Behavior, Vol. 5, Issue 7
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner
journal, October 2005
- Yamaguchi, T.; Aharon, G. S.; Sottosanto, J. B.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 44
The ins and outs of intracellular ion homeostasis: NHX-type cation/H + transporters
journal, December 2014
- Bassil, Elias; Blumwald, Eduardo
- Current Opinion in Plant Biology, Vol. 22
The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast
journal, February 1999
- Gaxiola, R. A.; Rao, R.; Sherman, A.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
Functional analyses of a putative plasma membrane Na+/H+ antiporter gene isolated from salt tolerant Helianthus tuberosus
journal, April 2014
- Li, Qing; Tang, Zhong; Hu, Yibing
- Molecular Biology Reports, Vol. 41, Issue 8
Vesicular trafficking and salinity responses in plants: Effect of Salinity on Endocytosis and Intracellular Trafficking
journal, August 2015
- Baral, Anirban; Shruthi, K. S.; Mathew, M. K.
- IUBMB Life, Vol. 67, Issue 9
Mechanisms of Salinity Tolerance
journal, June 2008
- Munns, Rana; Tester, Mark
- Annual Review of Plant Biology, Vol. 59, Issue 1
Molecular and functional comparisons of the vacuolar Na+/H+ exchangers originated from glycophytic and halophytic species
journal, February 2008
- Li, Jin-yao; He, Xiao-wei; Xu, Li
- Journal of Zhejiang University SCIENCE B, Vol. 9, Issue 2
Intracellular NHX-Type Cation/H+ Antiporters in Plants
journal, February 2014
- Reguera, Maria; Bassil, Elias; Blumwald, Eduardo
- Molecular Plant, Vol. 7, Issue 2
Root K+ Acquisition in Plants: The Arabidopsis thaliana Model
journal, July 2011
- Aleman, F.; Nieves-Cordones, M.; Martinez, V.
- Plant and Cell Physiology, Vol. 52, Issue 9
Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges: Rice two component nitrate transport
journal, June 2011
- Yan, Ming; Fan, Xiaorong; Feng, Huiming
- Plant, Cell & Environment, Vol. 34, Issue 8
Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance
journal, November 2006
- Leshem, Y.; Melamed-Book, N.; Cagnac, O.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 47