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Journal of Integrative Agriculture  2016, Vol. 15 Issue (11): 2497-2506    DOI: 10.1016/S2095-3119(16)61466-1
Physiology·Biochemistry·Cultivation·Tillage Advanced Online Publication | Current Issue | Archive | Adv Search |
Effects of short-term osmotic stress on leaf hydraulic conductivity and ZmPIPs mRNA accumulation in maize seedlings
WANG Wei-feng1, 2, ZONG Yu-zheng1, 3, ZHANG Sui-qi1
1 State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau/Institute of Soil and Water Conservation, Northwest A & F University, Yangling 712100, P.R.China
2 College of Forestry, Shanxi Agricultural University, Taigu 030801, P.R.China
3 College of Agriculture,Shanxi Agricultural University, Taigu 030801, P.R.China
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Abstract  Plants maintain water balance by varying hydraulic properties, and plasma membrane intrinsic proteins (PIPs) may be involved in this process.  Leaf xylem and root hydraulic conductivity and the mRNA contents of four highly expressed ZmPIP genes (ZmPIP1;1, ZmPIP1;2, ZmPIP2;2, and ZmPIP2;5) in maize (Zea mays) seedlings were investigated.  Under well-watered conditions, leaf hydraulic conductivity (Kleaf) varied diurnally and was correlated with whole-plant hydraulic conductivity.  Similar diurnal rhythms of leaf transpiration rate (E), Kleaf and root hydraulic conductivity (Kroot) in well-watered plants are important for maintaining whole-plant water balance.  After 2 h of osmotic stress treatment induced by 10% polyethylene glycol 6000, the Kroot of stressed plants decreased but Kleaf increased, compared with well-watered plants.  The mRNA contents of four ZmPIPs were significantly up-regulated in the leaves of stressed plants, especially for ZmPIP1;2.  Meanwhile, ZmPIP2;5 was significantly down-regulated in the roots of stressed plants.  After 4 h of osmotic stress treatment, the E and leaf xylem water potentials of stressed plants unexpectedly increased.  The increase in Kleaf and a partial recovery of Kroot may have contributed to this process.  The mRNA content of ZmPIP1;2 but not of the other three genes was up-regulated in roots at this time.  In summary, the mRNA contents of these four ZmPIPs associated with Kleaf and Kroot change in maize seedlings during short-term osmotic stress, especially for ZmPIP1;2 and ZmPIP2;5, which may help to further reveal the hydraulic resistance adjustment role of ZmPIPs.  
Keywords:  maize        short-term osmotic stress        hydraulic conductivity        ZmPIP  
Received: 14 March 2016   Accepted:
Fund: 

This study was financially supported by the National Natural Science Foundation of China (31400527, 31501276), the National High-Tech R&D Program of China (2011AA100504), the Project 111 of the Ministry of Education of China (B12007) and the Fund of State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, China (K318009902-1408).

Corresponding Authors:  ZHANG Sui-qi, Tel: +86-29-87010897, Fax: +86-29-87012210, E-mail: sqzhang@ms.iswc.ac.cn   

Cite this article: 

WANG Wei-feng, ZONG Yu-zheng, ZHANG Sui-qi. 2016. Effects of short-term osmotic stress on leaf hydraulic conductivity and ZmPIPs mRNA accumulation in maize seedlings. Journal of Integrative Agriculture, 15(11): 2497-2506.

Brundrett M C, Enstone D E, Peterson C A. 1988. A berberine-aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma, 146, 133–142.

Carpita N, Sabularse D, Montezinos D, Delmer D P. 1979. Determination of the pore size of cell walls of living plant cells. Science, 205, 1144–1147.

Chaumont F, Barrieu F, Jung R, Chrispeels M J. 2000. Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiology, 122, 1025–1034.

Chaumont F, Barrieu F, Wojcik E, Chrispeels M J, Jung R. 2001. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiology, 125, 1206–1215.

Christmann A, Weiler E W, Steudle E, Grill E. 2007. A hydraulic signal in root-to-shoot signalling of water shortage. Plant Journal, 52, 167–174.

Clarkson D T, Carvajal M, Henzler T, Waterhouse R N, Smyth A J, Cooke D T, Steudle E. 2000. Root hydraulic conductance: Diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany, 51, 61–70.

Cochard H, Venisse J S, Barigah T S, Brunel N, Herbette S, Guilliot A, Tyree M T, Sakr S. 2007. Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiology, 143, 122–133.

Fetter K, Van Wilder V, Moshelion M, Chaumont F. 2004. Interactions between plasma membrane aquaporins modulate their water channel activity. The Plant Cell, 16, 215–228.

Franks P J, Drake P L, Froend R H. 2007. Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell and Environment, 30, 19–30.

Hachez C, Heinen R B, Draye X, Chaumont F. 2008. The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Molecular Biology, 68, 337–353.

Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F. 2006. Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers. Plant Molecular Biology, 62, 305–323.

Hachez C, Veselov D, Ye Q, Reinhardt H, Knipfer T, Fricke W, Chaumont F. 2012. Short-term control of maize cell and root water permeability through plasma membrane aquaporin isoforms. Plant Cell and Environment, 35, 185–198.

Heinen R B, Ye Q, Chaumont F. 2009. Role of aquaporins in leaf physiology. Journal of Experimental Botany, 60, 2971–2985.

Henzler T, Waterhouse R N, Smyth A J, Carvajal M, Cooke D T, Schäffner A R, Steudle E, Clarkson D T. 1999. Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta, 210, 50–60.

Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güçlü J, Vinh J, Heyes J, Franck K I, Schäffner A R, Bouchez D. 2003. Role of a single aquaporin isoform in root water uptake. The Plant Cell, 15, 509–522.

Javot H, Maurel C. 2002. The role of aquaporins in root water uptake. Annals of Botany, 90, 301–313.

Kaldenhoff R, Ribas-Carbo M, Flexas J, Lovisolo C, Heckwolf M, Uehlein N. 2008. Aquaporins and plant water balance. Plant Cell and Environment, 31, 658–666.

Kim Y X, Steudle E. 2007. Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. Journal of Experimental Botany, 58, 4119–4129.

Lee S H, Chung G C, Jang J Y, Ahn S J, Zwiazek J J. 2012. Overexpression of PIP2;5 aquaporin alleviates effects of low root temperature on cell hydraulic conductivity and growth in Arabidopsis. Plant Physiology, 159, 479–488.

Lian H L, Yu X, Lane D, Sun W N, Tang Z C, Su W A. 2006. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Research, 16, 651–660.

Li G, Santoni V, Maurel C. 2014. Plant aquaporins: Roles in plant physiology. Biochimica et Biophysica Acta (BBA)-General Subjects, 1840, 1574–1582.

Lopez F, Bousser A, Sissoeff I, Gaspar M, Lachaise B, Hoarau J, Mahe A. 2003. Diurnal regulation of water transport and aquaporin gene expression in maize roots: Contribution of PIP2 proteins. Plant and Cell Physiology, 44, 1384–1395.

Martre P, Morillon R, Barrieu F, North G B, Nobel P S, Chrispeels M J. 2002. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology, 130, 2101–2110.

Maurel C, Simonneau T, Sutka M. 2010. The significance of roots as hydraulic rheostats. Journal of Experimental Botany, 61, 3191–3198.

North G B, Nobel P S. 1991. Changes in hydraulic conductivity and anatomy caused by drying and rewetting roots of Agave deserti (Agavaceae). American Journal of Botany, 78, 906–915.

Oertli J J. 1985. The response of plant cells to different forms of moisture stress. Journal of Plant Physiology, 121, 295–300.

Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F. 2009. Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: A trans-scale approach. Plant Physiology, 149, 2000–2012.

Sack L, Holbrook N M. 2006. Leaf hydraulics. Annual Review of Plant Biology, 57, 361–381.

Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M. 2008. Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant and Cell Physiology, 49, 30–39.

Secchi F, Lovisolo C, Schubert A. 2007. Expression of OePIP2.1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. Annals of Applied Biology, 150, 163–167.

Shatil-Cohen A, Attia Z, Moshelion M. 2011. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: A target of xylem-borne ABA? The Plant Journal, 67, 72–80.

Siefritz F, Tyree M T, Lovisolo C, Schubert A, Kaldenhoff R. 2002. PIP1 plasma membrane aquaporins in tobacco: From cellular effects to function in plants. The Plant Cell, 14, 869–876.

Sperry J S. 2011. Hydraulics of vascular water transport. In:  Wojtaszek P, ed., Mechanical Integration of Plant Cells and Plants. Springer, Berlin & Heidelberg. pp. 303–327.

Steudle E. 1994. Water transport across roots. Plant and Siol, 167, 79–90.

Steudle E. 2000. Water uptake by roots: Effects of water deficit. Journal of Experimental Botany, 51, 1531–1542.

Steudle E, Peterson C A. 1998. How does water get through roots? Journal of Experimental Botany, 49, 775–788.

Tao D, Li P H, Carter J V. 1983. Role of cell wall in freezing tolerance of cultured potato cells and their protoplasts. Physiologia Plantarum, 58, 527–532.

Tenhunen J D, Pearcy R W, Lange O L. 1987. Diurnal variations in leaf conductance and gas exchange in natural environments. In: Zeiger E, Farquhar G D, Cowan I R, eds., Stomatal Function. Stanford University Press, Stanford, CA. pp. 323–351.

Tsuda M, Tyree M T. 2000. Plant hydraulic conductance measured by the high pressure flow meter in crop plants. Journal of Experimental Botany, 51, 823–828.

Tyree M T, Patiño S, Bennink J, Alexander J. 1995. Dynamic measurements of roots hydraulic conductance using a high-pressure flowmeter in the laboratory and field. Journal of Experimental Botany, 46, 83–94.

Vandeleur R K, Mayo G, Shelden M C, Gilliham M, Kaiser B N, Tyerman S D. 2009. The role of plasma membrane intrinsic protein aquaporins in water transport through roots: Diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiology, 149, 445–460.

Vandeleur R K, Sullivan W, Athman A, Jordans C, Gilliham M, Kaiser B N, Tyerman S D. 2014. Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant, Cell & Environment, 37, 520–538.

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3, research0034.

Verslues P E, Agarwal M, Katiyar-Agarwal S, Zhu J H, Zhu J K. 2006. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal, 45, 523–539.

Wang W F, Yang X Q, Zhang S Q, Sun Y Y. 2013. The root cortex cell hydraulic conductivity is enhanced with increasing chromosome ploidy in wheat. Plant Physiology and Biochemistry, 68, 37–43.

Weig A, Deswarte C, Chrispeels M J. 1997. The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiology, 114, 1347–1357.

Wu Y, Liu X F, Wang W F, Zhang S Q, Xu B C. 2012. Calcium regulates the cell-to-cell water flow pathway in maize roots during variable water conditions. Plant Physiology and Biochemistry, 58, 212–219.

Yaaran A, Moshelion M. 2016. Role of aquaporins in a composite model of water transport in the leaf. International Journal of Molecular Sciences, 17, 1045.

Ye Q, Holbrook N M, Zwieniecki M A. 2008. Cell-to-cell pathway dominates xylem-epidermis hydraulic connection in Tradescantia fluminensis (Vell. Conc.) leaves. Planta, 227, 1311–1319.

Zelazny E, Borst J W, Muylaert M, Batoko H, Hemminga M A, Chaumont F. 2007. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proceedings of the National Academy of Sciences of the United States of America, 104, 12359–12364.

Zhang S Q, Zhou X P, Mu Z X, Shan L, Liu X F. 2009. Effects of different irrigation patterns on root growth and water use efficiency of maize. Transactions of the CSAE, 25, 1–6.
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