Potassium Uptake and Transport in Apple Roots Under Drought Stress
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摘要
As one of the most important mineral nutrient elements, potassium(K~+) plays an important role in many plant physiological processes and determines both the yield and quality of crops. There are two typical gene families that regulate K~+transport in higher plants, including K~+channels and K~+transporters. However, little is known about how these channels and transporters divide their work in response to drought stress. In this study, the hydroponic experiment was conducted on Malus hupehensis. The K~+content was found to decrease in response to drought stress in M. hupehensis, the aboveground decreased by 34.15% and the underground decreased by 3.97%. Meanwhile, the root morphology change was detected by scanning the root system. Under conditions of drought, the genes encoding K~+transporters were upregulated including MdCHX1.3, MdCHX4.11, MdCHX4.8, MdCHX4.9, Md HKT1, and MdHAK3.2. The net influx of K~+was inhibited by 19.47% with the action of K~+channel inhibitors(CsCl), however a significant decrease(80.99%; P < 0.05) was found in roots exposed to a PM H+-ATPase(orthovanadate) inhibitor by utilizing a non-invasive micro-test technique. The trend of H+efflux was similar to that of K~+. The data suggested that the positive influx of K~+through the transporter accounted for the main K~+uptake under drought stress. These results suggest that we can improve the uptake of K~+by purposely up-regulating specific K~+transporters under drought stress. This process may improve growth, yield, quality, and stress tolerance in apple trees.
As one of the most important mineral nutrient elements, potassium(K~+) plays an important role in many plant physiological processes and determines both the yield and quality of crops. There are two typical gene families that regulate K~+transport in higher plants, including K~+channels and K~+transporters. However, little is known about how these channels and transporters divide their work in response to drought stress. In this study, the hydroponic experiment was conducted on Malus hupehensis. The K~+content was found to decrease in response to drought stress in M. hupehensis, the aboveground decreased by 34.15% and the underground decreased by 3.97%. Meanwhile, the root morphology change was detected by scanning the root system. Under conditions of drought, the genes encoding K~+transporters were upregulated including MdCHX1.3, MdCHX4.11, MdCHX4.8, MdCHX4.9, Md HKT1, and MdHAK3.2. The net influx of K~+was inhibited by 19.47% with the action of K~+channel inhibitors(CsCl), however a significant decrease(80.99%; P < 0.05) was found in roots exposed to a PM H+-ATPase(orthovanadate) inhibitor by utilizing a non-invasive micro-test technique. The trend of H+efflux was similar to that of K~+. The data suggested that the positive influx of K~+through the transporter accounted for the main K~+uptake under drought stress. These results suggest that we can improve the uptake of K~+by purposely up-regulating specific K~+transporters under drought stress. This process may improve growth, yield, quality, and stress tolerance in apple trees.
As one of the most important mineral nutrient elements, potassium(K~+) plays an important role in many plant physiological processes and determines both the yield and quality of crops. There are two typical gene families that regulate K~+transport in higher plants, including K~+channels and K~+transporters. However, little is known about how these channels and transporters divide their work in response to drought stress. In this study, the hydroponic experiment was conducted on Malus hupehensis. The K~+content was found to decrease in response to drought stress in M. hupehensis, the aboveground decreased by 34.15% and the underground decreased by 3.97%. Meanwhile, the root morphology change was detected by scanning the root system. Under conditions of drought, the genes encoding K~+transporters were upregulated including MdCHX1.3, MdCHX4.11, MdCHX4.8, MdCHX4.9, Md HKT1, and MdHAK3.2. The net influx of K~+was inhibited by 19.47% with the action of K~+channel inhibitors(CsCl), however a significant decrease(80.99%; P < 0.05) was found in roots exposed to a PM H+-ATPase(orthovanadate) inhibitor by utilizing a non-invasive micro-test technique. The trend of H+efflux was similar to that of K~+. The data suggested that the positive influx of K~+through the transporter accounted for the main K~+uptake under drought stress. These results suggest that we can improve the uptake of K~+by purposely up-regulating specific K~+transporters under drought stress. This process may improve growth, yield, quality, and stress tolerance in apple trees.
引文
Abbasi,H.,Jamil,M.,Haq,A.,Ali,S.,Ahmad,R.,Malik,Z.,2016.Salt stress manifestation on plants,mechanism of salt tolerance and potassium role in alleviating it:a review.Zemdirbyste,103:229-238.
Alvarez-Pizarro,J.C.,Gomes-Filho,E.,Prisco,J.T.,Grossi-de-Sá,M.F.,Oliveira-Neto,O.B.D.,2011.NH4+-stimulated low-K+uptake is associated with the induction of H+extrusion by the plasma membrane H+-ATPase in sorghum roots under K+deficiency.J Plant Physiol,168:1617-1626.
Bai,T.H.,Ma,F.W.,Li,C.Y.,Shu,H.R.,Han,M.Y.,Wang,K.,2008.Physiological responses and analysis of tolerance of apple rootstocks to root-zone hypoxia stress.Sci Agric Sin,41:4140-4148.
Britto,D.T.,Kronzucker,H.J.,2008.Cellular mechanisms of potassium transport in plants.Physiol Plant,133:637-650.
Cellier,F.,Genevieve,C.,Ricaud,L.,Doan,T.L.,Marc,L.,Fran?oise,G.,Francine,C.,2004.Characterization of At CHX17,a member of the cation/H+exchangers,CHX family,from Arabidopsis thaliana suggests a role in K+homeostasis.Plant J,39:834-846.
Chen,S.C.,Wang,M.,Wang,J.,Gao,Y.,Liu,Z.,Wang,X.,2017.Response of seed germination and seedling physiological characteristics of Medicago sativa to the simulated osmotic potential of PEG6000.Chin J Appl Ecol,9:2923-2931.
Chen,Z.,Cuin,T.A.,Zhou,M.,Twomey,A.,Naidu,B.P.,Shabala,S.,2007.Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance.J Exp Bot,58:4245-4255.
Clarkson,D.T.,Hanson,J.B.,1980.The mineral nutrition of higher plants.Annu Rev Plant Physiol,31:239-298.
Cuin,T.A.,Betts,S.A.,Chalmandrier,R.,Shabala,S.,2008.A root’s ability to retain K+correlates with salt tolerance in wheat.J Exp Bot,59:2697-2706.
Cuin,T.A.,Zhou,M.,Parsons,D.,Shabala,S.,2011.Genetic behaviour of physiological traits conferring cytosolic K+/Na+homeostasis in wheat.Plant Biol,14:438-446.
Dell’Orto,M.,Santi,S.,Nisi,P.D.,Cesco,S.,Varanini,Z.,Zocchi,G.,Pinton,R.,2000.Development of Fe-deficiency responses in cucumber(Cucumis sativus L.)roots:involvement of plasma membrane H+-ATPase activity.J Exp Bot,51:695-701.
Dionisio-Sese,M.L.,Tobita,S.,1998.Antioxidant responses of rice seedlings to salinity stress.Plant Sci,135:1-9.
Epstein,E.,Rains,D.W.,Elzam,O.E.,1963.Resolution of dual mechanisms of potassium absorption by barley roots.Proc Natl Acad Sci,49:684-692.
Frensch,J.,Steudle,E.,1989.Axial and radial hydraulic resistance to roots of maize(Zea mays L.).Plant Physiol,91:719-726.
Gambale,F.,Uozumi,N.,2006.Properties of shaker-type potassium channels in higher plants.J Membrane Bio,210:1-19.
Gaxiola,R.A.,Li,J.,Undurraga,S.,Dang,L.M.,Allen,G.J.,Alper,S.L.,Fink,G.R.,2001.Drought-and salt-tolerant plants result from overexpression of the AVP1 H+-pump.Proc Natl Acad Sci USA,98:11444-11449.
Gierth,M.,Maser,P.,2007.Potassium transporters in plants-involvement in K+acquisition,redistribution and homeostasis.FEBS Lett,581:2348-2356.
Gullo,M.A.,Salleo,S.,1993.Different vulnerabilities of Quercus ilex L.to freeze-and summer drought-induced xylem embolism:an ecological interpretation.Plant Cell Environ,16:511-519.
Haling,R.E.,Richardson,A.E.,Culvenor,R.A.,Lambers,H.,Simpson,R.J.,2010.Root morphology,root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity.Plant Soil,335:457-468.
He,J.L.,Qin,J.,Long,L.Y.,Ma,Y.L.,Li,H.,Li,K.,Jiang,X.N.,Liu,T.X.,Polle,A.,Liang,Z.S.,Luo,Z.B.,2011.Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus×canescens.Physiol Plant,143:50-63.
Hsiao,T.C.,1973.Plant responses to water stress.Annu Rev Plant Physiol Plant Mol Biol,24:519-570.
Hu,L.X.,Wang,Z.L.,Huang,B.R.,2013.Effects of cytokinin and potassium on stomatal and photosynthetic recovery of Kentucky bluegrass from drought stress.Crop Sci,53:221-231.
Hu,Y.C.,Schmidhalter,U.,2005.Drought and salinity:a comparison of their effects on mineral nutrition of plants.J Plant Nutr Soil Sci,168:541-549.
Huang,Y.,Zhao,L.,Kong,Q.,Cheng,F.,Niu,M.,Xie,J.,Nawaz,M.A.,Bie,Z.,2016.Comprehensive mineral nutrition analysis of watermelon grafted onto two different rootstocks.Hortic Plant J,2:105-113.
Jupp,A.P.,Newman,E.I.,1987.Morphological and anatomical effects of severe drought on the roots of Lolium perenne L.New Phytol,105:393-402.
Lebaudy,A.,Very,A.A.,Sentenac,H.,2007.K+channel activity in plants:genes,regulations and functions.FEBS Lett,581:2357-2366.
Li,J.,Chen,J.,2017.Citrus fruit-cracking:causes and occurrence.Hortic Plant J,3:255-260.
Li,Q.,Li,B.H.,Kronzucker,H.J.,Shi,W.M.,2010.Root growth inhibition by NH4+in Arabidopsis is mediated by the root tip and is linked to NH4+efflux and GMPase activity.Plant Cell Environ,33:1529-1542.
Luo,J.,Qin,J.,He,F.,Li,H.,Liu,T.,Polle,A.,Peng,C.,Luo,Z.B.,2013.Net fluxes of ammonium and nitrate in association with H+fluxes in fine roots of Populus popularis.Planta,237:919-931.
Marschner,H.,1995.Mineral Nutrition of Higher Plants,2nd ed Academic Press Ltd,London.
Maser,P.,Thimine,S.,Schroeder,J.I.,Ward,J.M.,Hirschi,K.,Sze,H.,Talke,I.N.,Amtmann,A.,Maathuis,F.J.M.,2001.Phylogenetic relationships within cation transporter families of Arabidopsis.Plant Physiol,126:1646-1667.
McInenly,L.E.,Merrill,E.H.,Cahill,J.F.,Juma,N.G.,2010.Festuca campestris alters root morphology and growth in response to simulated grazing and nitrogen form.Funct Ecol,24:283-292.
Palmgren,M.G.,2001.Plant plasma membrane H+-ATPases:powerhouses for nutrient uptake.Annu Rev Plant Biol,52:817-845.
Rubio,B.,Nombela,M.A.,Vilas,F.,2000.Geochemistry of major and trace elements in sediments of the Ria de Vigo(NW Spain):an assessment of metal pollution.Mar Pollut Bull,40:968-980.
Sahr,T.,Voigt,G.,Paretzke,H.G.,Schramel,P.,Ernst,D.,2005.Caesium-affected gene expression in Arabidopsis thaliana.New Phytol,165:747-754.
Santi,S.,Schmidt,W.,2009.Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots.New Phytol,183:1072-1084.
Schikora,A.,Schmidt,W.,2002.Formation of transfer cells and H+-ATPase expression in tomato roots under P and Fe deficiency.Planta,215:304-311.
Shabala,S.,2003.Regulation of potassium transport in leaves:from molecular to tissue level.Annu Bot,92:627-634.
Shabala,S.,Pottosin,I.,2014.Regulation of potassium transport in plants under hostile conditions:implications for abiotic and biotic stress tolerance.Physiol Plant,151:257-279.
Shen,C.,Ding,Y.,Lei,X.,Zhao,P.,Wang,S.,Xu,Y.,Dong,C.,2016.Effects of foliar potassium fertilization on fruit growth rate,potassium accumulation,yield,and quality of‘Kousui’Japanese pear.Horttechnology,26:270-277.
Shi,G.,Xia,S.,Ye,J.,Huang,Y.,Liu,C.,Zhang,Z.,2015.PEG-simulated drought stress decreases cadmium accumulation in castor bean by altering root morphology.Environ Exp Bot,111:127-134.
Smethurst,C.F.,Rix,K.,Garnett,T.,Auricht,G.,Bayart,A.,Lane,P.,Wilson,S.J.,Shabala,S.,2008.Multiple traits associated with salt tolerance in lucerne:revealing the underlying cellular mechanisms.Funct Plant Biol,35:640-650.
Steudle,E.,2000.Water uptake by roots:effects of water deficit.J Exp Bot,51:1531-1542 stress-mitigating effects in barley genotypes contrasting in their salt tolerance.J Exp Bot,58:4245-4255.
Sze,H.,1985.H+-Translocating ATPases:advances using membrane-vesicles.Annu Rev Plant Physiol,36:175-208.
Very,A.A.,Sentenac,H.,2003.Molecular mechanisms and regulation of K+transport in higher plants.Annu Rev Plant Biol,54:575-603.
Victoria,V.,Jorge,B.,Gabriela,S.,Nicolas,D.A.,Gabriela,A.,2015.Root hydraulic conductivity and adjustments in stomatal conductance:hydraulic strategy in response to salt stress in a halotolerant species.AoB Plants,7:136-147.
Wang,Y.,Wu,W.H.,2013.Potassium transport and signaling in higher plant.Annu Rev Plant Biol,64:451-476.
Wegner,L.H.,2015.Interplay of water and nutrient transport:a whole plant perspective.Prog Bot,76:109-141.
Xu,Y.,Sun,T.,Yin,L.P.,2006.Application of non-invasive microsensing system to simultaneously measure both H+and O2-fluxes around the pollen tube.J Integr Plant Biol,48:823-831.
Alvarez-Pizarro,J.C.,Gomes-Filho,E.,Prisco,J.T.,Grossi-de-Sá,M.F.,Oliveira-Neto,O.B.D.,2011.NH4+-stimulated low-K+uptake is associated with the induction of H+extrusion by the plasma membrane H+-ATPase in sorghum roots under K+deficiency.J Plant Physiol,168:1617-1626.
Bai,T.H.,Ma,F.W.,Li,C.Y.,Shu,H.R.,Han,M.Y.,Wang,K.,2008.Physiological responses and analysis of tolerance of apple rootstocks to root-zone hypoxia stress.Sci Agric Sin,41:4140-4148.
Britto,D.T.,Kronzucker,H.J.,2008.Cellular mechanisms of potassium transport in plants.Physiol Plant,133:637-650.
Cellier,F.,Genevieve,C.,Ricaud,L.,Doan,T.L.,Marc,L.,Fran?oise,G.,Francine,C.,2004.Characterization of At CHX17,a member of the cation/H+exchangers,CHX family,from Arabidopsis thaliana suggests a role in K+homeostasis.Plant J,39:834-846.
Chen,S.C.,Wang,M.,Wang,J.,Gao,Y.,Liu,Z.,Wang,X.,2017.Response of seed germination and seedling physiological characteristics of Medicago sativa to the simulated osmotic potential of PEG6000.Chin J Appl Ecol,9:2923-2931.
Chen,Z.,Cuin,T.A.,Zhou,M.,Twomey,A.,Naidu,B.P.,Shabala,S.,2007.Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance.J Exp Bot,58:4245-4255.
Clarkson,D.T.,Hanson,J.B.,1980.The mineral nutrition of higher plants.Annu Rev Plant Physiol,31:239-298.
Cuin,T.A.,Betts,S.A.,Chalmandrier,R.,Shabala,S.,2008.A root’s ability to retain K+correlates with salt tolerance in wheat.J Exp Bot,59:2697-2706.
Cuin,T.A.,Zhou,M.,Parsons,D.,Shabala,S.,2011.Genetic behaviour of physiological traits conferring cytosolic K+/Na+homeostasis in wheat.Plant Biol,14:438-446.
Dell’Orto,M.,Santi,S.,Nisi,P.D.,Cesco,S.,Varanini,Z.,Zocchi,G.,Pinton,R.,2000.Development of Fe-deficiency responses in cucumber(Cucumis sativus L.)roots:involvement of plasma membrane H+-ATPase activity.J Exp Bot,51:695-701.
Dionisio-Sese,M.L.,Tobita,S.,1998.Antioxidant responses of rice seedlings to salinity stress.Plant Sci,135:1-9.
Epstein,E.,Rains,D.W.,Elzam,O.E.,1963.Resolution of dual mechanisms of potassium absorption by barley roots.Proc Natl Acad Sci,49:684-692.
Frensch,J.,Steudle,E.,1989.Axial and radial hydraulic resistance to roots of maize(Zea mays L.).Plant Physiol,91:719-726.
Gambale,F.,Uozumi,N.,2006.Properties of shaker-type potassium channels in higher plants.J Membrane Bio,210:1-19.
Gaxiola,R.A.,Li,J.,Undurraga,S.,Dang,L.M.,Allen,G.J.,Alper,S.L.,Fink,G.R.,2001.Drought-and salt-tolerant plants result from overexpression of the AVP1 H+-pump.Proc Natl Acad Sci USA,98:11444-11449.
Gierth,M.,Maser,P.,2007.Potassium transporters in plants-involvement in K+acquisition,redistribution and homeostasis.FEBS Lett,581:2348-2356.
Gullo,M.A.,Salleo,S.,1993.Different vulnerabilities of Quercus ilex L.to freeze-and summer drought-induced xylem embolism:an ecological interpretation.Plant Cell Environ,16:511-519.
Haling,R.E.,Richardson,A.E.,Culvenor,R.A.,Lambers,H.,Simpson,R.J.,2010.Root morphology,root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity.Plant Soil,335:457-468.
He,J.L.,Qin,J.,Long,L.Y.,Ma,Y.L.,Li,H.,Li,K.,Jiang,X.N.,Liu,T.X.,Polle,A.,Liang,Z.S.,Luo,Z.B.,2011.Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus×canescens.Physiol Plant,143:50-63.
Hsiao,T.C.,1973.Plant responses to water stress.Annu Rev Plant Physiol Plant Mol Biol,24:519-570.
Hu,L.X.,Wang,Z.L.,Huang,B.R.,2013.Effects of cytokinin and potassium on stomatal and photosynthetic recovery of Kentucky bluegrass from drought stress.Crop Sci,53:221-231.
Hu,Y.C.,Schmidhalter,U.,2005.Drought and salinity:a comparison of their effects on mineral nutrition of plants.J Plant Nutr Soil Sci,168:541-549.
Huang,Y.,Zhao,L.,Kong,Q.,Cheng,F.,Niu,M.,Xie,J.,Nawaz,M.A.,Bie,Z.,2016.Comprehensive mineral nutrition analysis of watermelon grafted onto two different rootstocks.Hortic Plant J,2:105-113.
Jupp,A.P.,Newman,E.I.,1987.Morphological and anatomical effects of severe drought on the roots of Lolium perenne L.New Phytol,105:393-402.
Lebaudy,A.,Very,A.A.,Sentenac,H.,2007.K+channel activity in plants:genes,regulations and functions.FEBS Lett,581:2357-2366.
Li,J.,Chen,J.,2017.Citrus fruit-cracking:causes and occurrence.Hortic Plant J,3:255-260.
Li,Q.,Li,B.H.,Kronzucker,H.J.,Shi,W.M.,2010.Root growth inhibition by NH4+in Arabidopsis is mediated by the root tip and is linked to NH4+efflux and GMPase activity.Plant Cell Environ,33:1529-1542.
Luo,J.,Qin,J.,He,F.,Li,H.,Liu,T.,Polle,A.,Peng,C.,Luo,Z.B.,2013.Net fluxes of ammonium and nitrate in association with H+fluxes in fine roots of Populus popularis.Planta,237:919-931.
Marschner,H.,1995.Mineral Nutrition of Higher Plants,2nd ed Academic Press Ltd,London.
Maser,P.,Thimine,S.,Schroeder,J.I.,Ward,J.M.,Hirschi,K.,Sze,H.,Talke,I.N.,Amtmann,A.,Maathuis,F.J.M.,2001.Phylogenetic relationships within cation transporter families of Arabidopsis.Plant Physiol,126:1646-1667.
McInenly,L.E.,Merrill,E.H.,Cahill,J.F.,Juma,N.G.,2010.Festuca campestris alters root morphology and growth in response to simulated grazing and nitrogen form.Funct Ecol,24:283-292.
Palmgren,M.G.,2001.Plant plasma membrane H+-ATPases:powerhouses for nutrient uptake.Annu Rev Plant Biol,52:817-845.
Rubio,B.,Nombela,M.A.,Vilas,F.,2000.Geochemistry of major and trace elements in sediments of the Ria de Vigo(NW Spain):an assessment of metal pollution.Mar Pollut Bull,40:968-980.
Sahr,T.,Voigt,G.,Paretzke,H.G.,Schramel,P.,Ernst,D.,2005.Caesium-affected gene expression in Arabidopsis thaliana.New Phytol,165:747-754.
Santi,S.,Schmidt,W.,2009.Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots.New Phytol,183:1072-1084.
Schikora,A.,Schmidt,W.,2002.Formation of transfer cells and H+-ATPase expression in tomato roots under P and Fe deficiency.Planta,215:304-311.
Shabala,S.,2003.Regulation of potassium transport in leaves:from molecular to tissue level.Annu Bot,92:627-634.
Shabala,S.,Pottosin,I.,2014.Regulation of potassium transport in plants under hostile conditions:implications for abiotic and biotic stress tolerance.Physiol Plant,151:257-279.
Shen,C.,Ding,Y.,Lei,X.,Zhao,P.,Wang,S.,Xu,Y.,Dong,C.,2016.Effects of foliar potassium fertilization on fruit growth rate,potassium accumulation,yield,and quality of‘Kousui’Japanese pear.Horttechnology,26:270-277.
Shi,G.,Xia,S.,Ye,J.,Huang,Y.,Liu,C.,Zhang,Z.,2015.PEG-simulated drought stress decreases cadmium accumulation in castor bean by altering root morphology.Environ Exp Bot,111:127-134.
Smethurst,C.F.,Rix,K.,Garnett,T.,Auricht,G.,Bayart,A.,Lane,P.,Wilson,S.J.,Shabala,S.,2008.Multiple traits associated with salt tolerance in lucerne:revealing the underlying cellular mechanisms.Funct Plant Biol,35:640-650.
Steudle,E.,2000.Water uptake by roots:effects of water deficit.J Exp Bot,51:1531-1542 stress-mitigating effects in barley genotypes contrasting in their salt tolerance.J Exp Bot,58:4245-4255.
Sze,H.,1985.H+-Translocating ATPases:advances using membrane-vesicles.Annu Rev Plant Physiol,36:175-208.
Very,A.A.,Sentenac,H.,2003.Molecular mechanisms and regulation of K+transport in higher plants.Annu Rev Plant Biol,54:575-603.
Victoria,V.,Jorge,B.,Gabriela,S.,Nicolas,D.A.,Gabriela,A.,2015.Root hydraulic conductivity and adjustments in stomatal conductance:hydraulic strategy in response to salt stress in a halotolerant species.AoB Plants,7:136-147.
Wang,Y.,Wu,W.H.,2013.Potassium transport and signaling in higher plant.Annu Rev Plant Biol,64:451-476.
Wegner,L.H.,2015.Interplay of water and nutrient transport:a whole plant perspective.Prog Bot,76:109-141.
Xu,Y.,Sun,T.,Yin,L.P.,2006.Application of non-invasive microsensing system to simultaneously measure both H+and O2-fluxes around the pollen tube.J Integr Plant Biol,48:823-831.