Ectopic expression of a rice plasma membrane intrinsic protein (OsPIP1;3) promotes plant growth and water uptake

被引:60
作者
Liu, Siyu [1 ]
Fukumoto, Tatsuya [2 ]
Gena, Patrizia [3 ]
Feng, Peng [1 ]
Sun, Qi [1 ]
Li, Qiang [1 ]
Matsumoto, Tadashi [2 ]
Kaneko, Toshiyuki [4 ]
Zhang, Hang [1 ]
Zhang, Yao [5 ]
Zhong, Shihua [6 ]
Zeng, Weizhong [7 ]
Katsuhara, Maki [4 ]
Kitagawa, Yoshichika [2 ]
Wang, Aoxue [5 ]
Calamita, Giuseppe [3 ]
Ding, Xiaodong [1 ]
机构
[1] Northeast Agr Univ, Key Lab Agr Biol Funct Genes, Harbin 150030, Peoples R China
[2] Akita Prefectural Univ, Grad Sch Bioresource Sci, Akita 0100195, Japan
[3] Univ Bari Aldo Moro, Dept Biosci Biotechnol & Biopharmaceut, Bari, Italy
[4] Okayama Univ, Res Inst Bioresources, Kurashiki, Okayama 7100046, Japan
[5] Northeast Agr Univ, Coll Hort, Harbin 150030, Peoples R China
[6] Univ Texas Southwestern Med Ctr Dallas, Dept Biochem, Dallas, TX 75390 USA
[7] Univ Texas Southwestern Med Ctr Dallas, Dept Biophys, Dallas, TX 75390 USA
基金
中国国家自然科学基金;
关键词
aquaporin; water; nitrate; carbon dioxide; permeability; hydraulic conductivity; membrane transport; plant growth; ROOT HYDRAULIC CONDUCTANCE; TOBACCO AQUAPORIN NTAQP1; SLAC1 ANION CHANNEL; SOYBEAN NODULIN 26; MESOPHYLL CONDUCTANCE; FUNCTIONAL RECONSTITUTION; DROUGHT TOLERANCE; PIP2; AQUAPORINS; CO2; GENE;
D O I
10.1111/tpj.14662
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Plasma membrane intrinsic proteins (PIPs) are known to be major facilitators of the movement of a number of substrates across cell membranes. From a drought-resistant cultivar of Oryza sativa (rice), we isolated an OsPIP1;3 gene single-nucleotide polymorphism (SNP) that is mostly expressed in rice roots and is strongly responsive to drought stress. Immunocytochemistry showed that OsPIP1;3 majorly accumulated on the proximal end of the endodermis and the cell surface around the xylem. Expression of GFP-OsPIP1;3 alone in Xenopus oocytes or rice protoplasts showed OsPIP1;3 mislocalization in the endoplasmic reticulum (ER)-like neighborhood, whereas co-expression of OsPIP2;2 recruited OsPIP1;3 to the plasma membrane and led to a significant enhancement of water permeability in oocytes. Moreover, reconstitution of 10xHis-OsPIP1;3 in liposomes demonstrated water channel activity, as revealed by stopped-flow light scattering. Intriguingly, by patch-clamp technique, we detected significant NO3- conductance of OsPIP1;3 in mammalian cells. To investigate the physiological functions of OsPIP1;3, we ectopically expressed the OsPIP1;3 gene in Nicotiana benthamiana (tobacco). The transgenic tobacco plants exhibited higher photosynthesis rates, root hydraulic conductivity (Lp(r)) and water-use efficiency, resulting in a greater biomass and a higher resistance to water deficit than the wild-type did. Further experiments suggested that heterologous expression of OsPIP1;3 in cyanobacterium altered bacterial growth under different conditions of CO2 gas supply. Overall, besides shedding light on the multiple functions played by OsPIP1;3, this work provides insights into the translational value of plant AQPs.
引用
收藏
页码:779 / 796
页数:18
相关论文
共 79 条
[1]   Diversity and evolution of membrane intrinsic proteins [J].
Abascal, Federico ;
Irisarri, Iker ;
Zardoya, Rafael .
BIOCHIMICA ET BIOPHYSICA ACTA-GENERAL SUBJECTS, 2014, 1840 (05) :1468-1481
[2]   Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress [J].
Aharon, R ;
Shahak, Y ;
Wininger, S ;
Bendov, R ;
Kapulnik, Y ;
Galili, G .
PLANT CELL, 2003, 15 (02) :439-447
[3]   Whole gene family expression and drought stress regulation of aquaporins [J].
Alexandersson, E ;
Fraysse, L ;
Sjövall-Larsen, S ;
Gustavsson, S ;
Fellert, M ;
Karlsson, M ;
Johanson, U ;
Kjellbom, P .
PLANT MOLECULAR BIOLOGY, 2005, 59 (03) :469-484
[4]   Functional characterization of drought-responsive aquaporins in Populus balsamifera and Populus simonii x balsamifera clones with different drought resistance strategies [J].
Almeida-Rodriguez, Adriana M. ;
Cooke, Janice E. K. ;
Yeh, Francis ;
Zwiazek, Janusz J. .
PHYSIOLOGIA PLANTARUM, 2010, 140 (04) :321-333
[5]  
BABA A, 1986, PLANT CELL PHYSIOL, V27, P463
[6]   Heterotetramerization of Plant PIP1 and PIP2 Aquaporins Is an Evolutionary Ancient Feature to Guide PIP1 Plasma Membrane Localization and Function [J].
Bienert, Manuela D. ;
Diehn, Till A. ;
Richet, Nicolas ;
Chaumont, Francois ;
Bienert, Gerd P. .
FRONTIERS IN PLANT SCIENCE, 2018, 9
[7]   Functional reconstitution and characterization of AqpZ, the E-coli water channel protein [J].
Borgnia, MJ ;
Kozono, D ;
Calamita, G ;
Maloney, PC ;
Agre, P .
JOURNAL OF MOLECULAR BIOLOGY, 1999, 291 (05) :1169-1179
[8]   MOLECULAR-CLONING AND CHARACTERIZATION OF AQPZ, A WATER CHANNEL FROM ESCHERICHIA-COLI [J].
CALAMITA, G ;
BISHAI, WR ;
PRESTON, GM ;
GUGGINO, WB ;
AGRE, P .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1995, 270 (49) :29063-29066
[9]   Water permeability of rat liver mitochondria: A biophysical study [J].
Calamita, Giuseppe ;
Gena, Patrizia ;
Meleleo, Damela ;
Ferri, Domenico ;
Svelto, Maria .
BIOCHIMICA ET BIOPHYSICA ACTA-BIOMEMBRANES, 2006, 1758 (08) :1018-1024
[10]   Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity [J].
Chaumont, F ;
Barrieu, F ;
Jung, R ;
Chrispeels, MJ .
PLANT PHYSIOLOGY, 2000, 122 (04) :1025-1034