Aquaporins and the control of the water status in coffee plants

Santos, Adriana Brombini dos; Mazzafera, Paulo

Abstract

Six aquaporin (AQP) homologues were identified in three coffee species (Coffea arabica, C. Canephora, and C. racemosa), including four plasma membrane intrinsic proteins (PIP1;1, PIP1;2, PIP2;1, and PIP2;2) and two tonoplast intrinsic proteins (TIP1;1 and TIP1;2). In order to better understand the role of these genes in coffee, C. arabica cvs Catuaí and Mundo Novo, C. canephora cv. Apoatã, and a graft of Mundo Novo on Apoatã were water stressed, and the expression levels of PIP1;2, PIP2;1, PIP2;2, and TIP1;2 were analyzed in the roots and leaves. The expression of PIP2;1 and PIP2;2 was clearly up-regulated in the leaves and roots by water deficit, suggesting the possible involvement of these genes in controlling the water status of plants and in the post-stress recovery of irrigated plants. The most strongly induced expression in roots was found in both grafted and non-grafted Apoatã plants. Interestingly, the level of PIP2;1 transcripts in roots continued to rise even after the plants were watered and were, therefore, no longer subjected to the water stress, suggesting that this gene may be actively involved in the regulation of water uptake in coffee tree roots, especially when there is a water deficit in the soil.

aquaporins; PIPs; Coffea arabica; Coffea canephora; water stress; root

Agre P, Sasaki, S, Chrispeels MJ (1993) Aquaporins: a family of water channel proteins. American Journal of Physiology - Renal Physiology 265:F461-F461.
Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439-447.
Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Molecular Biology 59:469-484.
Aroca R, Ferrante A, Vernieri P, Chrispeels MJ (2006) Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Annals of Botany 98:1301-1310.
Aroca R, Porcel R, Ruiz-Lozano MJ (2012) Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany 63:43-57.
Baiges I, Schaffner AR, Mas A (2001) Eight cDNA encoding putative aquaporins in Vitis hybrid Richter-110 and their differential expression. Journal of Experimental Botany 52:1949-1951.
Barsalobres-Cavallari CF, Severino FE, Maluf MP, Maia IG (2009) Identification of suitable internal control genes for expression studies in Coffea arabica under different experimental conditions. BMC Molecular Biology 10:1.
Bogeat-Triboulot MB, Brosche M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman JF, Polle A, Kangasjärvi J, Dreyer E (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiology 143:876-892.
Cenci A, Combes MC, Lashermes P (2010) Comparative sequence analyses indicate that Coffea (Asterids) and Vitis (Rosids) derive from the same paleo-hexaploid ancestral genome. Molecular Genetics and Genomics 283:493-501.
Chaumont F, Barrieu F, Jung R, Chrispeels MJ (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 MJ, Jung, R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiology 125:1206-1215.
DaMatta F, Ramalho J (2006) Impacts of drought and temperature stress on coffee physiology and production: a review. Brazilian Journal Plant Physiology 18:55-81.
DaMatta FM, Chaves ARM, Pinheiro HA, Ducatti C, Loureiro ME (2003) Drought tolerance of two field-grown clones of Coffea canephora Plant Science 164:111-117.
Danielson JAH, Johanson U (2008) Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens BMC Plant Biology 8:45.
Dias PC, Araujo WL, Moraes GABK, Barros RS, DaMatta FM (2007) Morphological and physiological responses of two coffee progenies to soil water availability. Journal of Plant Physiology 164:1639-1647.
Fahl JI, Carelli MLC, Gallo PB, Costa WM, Novo MCSS (1998) Enxertia de Coffea arabica sobre progênies de C. canephora e de C. congensis no crescimento, nutrição mineral e produção. Bragantia 52:297-312.
Fahl JI, Carelli MLC, Menezes HC, Gallo PB Trivelin PCO (2001) Gas exchage, growth, yield and beverage quality of Coffea arabica cultivars grafted on to C. canephora and C. congensis Experimental Agriculture 37:241-252.
Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215-228.
Forrest KL, Bhave M (2008) The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Functional and Integrative Genomics 8:115-133.
Galmes J, Pou A, Alsina MM, Tomas M, Medrano H, Flexas J (2007) Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta 226:671-681.
Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu MH, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Research 16:277-286.
Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: Characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biology 9:134. doi: 10.1186/1471-2229-9-134
Guyot R, Lefebvre-Pautigny F, Tranchant-Dubreuil C, Rigoreau M, Hamon P, Leroy T, Hamon S, Poncet V, Crouzillat D, de Kochko A (2012) Ancestral synteny shared between distantly-related plant species from the asterid (Coffea canephora and Solanum sp.) and rosid (Vitis vinifera) clades. BMC Genomics 13: 103. doi: 10.1186/1471-2164-13-103.
Hachez C, Heinen RB, 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.
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, pp.95-98.
Huang XQ (1992) A contig assembly program based on sensitive detection of fragment overlaps. Genomics 14:18-25.
Jang JY, Kim DG, Kim YO, Kim JS, Kang HS (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana Plant Molecular Biology 54:713-725.
Jang JY, Lee SH, Rhee JY, Chung GC, Ahn SJ, Kang H (2007a) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Molecular Biology 64:621-632.
Jang JY, Rhee JY, Kim DG, Chung GC, Lee JH, Kang H (2007b) Ectopic expression of a foreign aquaporin disrupts the natural expression patterns of endogenous aquaporin genes and alters plant responses to different stress conditions. Plant and Cell Physiology 48:1331-1339.
Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509-522.
Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiology 126:1358-1369.
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. doi: 10.1111/j.1365-3040.2008.01792.x
Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant and Cell Physiology 43:885-893.
Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant and Cell Physiology 45:481-489.
Lin CW, Mueller LA, McCarthy J, Crouzillat D, Petiard V, Tanksley SD (2005) Coffee and tomato share common gene repertoires as revealed by deep sequencing of seed and cherry transcripts. Theoretical and Applied Genetics 112:114-130.
Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant, Cell and Environment 28:85-96.
Mahdieh M, Mostajeran A, Horie T, Katsuhara M (2008) Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant and Cell Physiology 49:801-813.
Manuel Ruiz-Lozano J, del Mar Alguacil M, Barzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Molecular Biology 70:565-579.
Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology 130:2101-2110.
Maurel C, Verdoucq L, Luu D-T, Santoni, V (2008) Plant aquaporins: Membrane channels with multiple integrated functions. Annual Review of Plant Biology 59:595-624.
Mondego JMC, Vidal RO, Carazzolle MF, Tokuda EK, Parizzi LP, Costa GG, Pereira LF, Andrade AC, Colombo CA, Vieira LG, Pereira GA, Brazilian Coffee Genome Project Consortium (2011) An EST-based analysis identifies new genes and reveals distinctive gene expression features of Coffea arabica and Coffea canephora BMC Plant Biology 11:30. doi: 10.1186/1471-2229-11-30.
Moraes MV, Franco CM (1973) Método expedito para enxertia em café. Instituto Brasileiro do Café, Rio de Janeiro. 8p.
Morais H, Caramori PH, Koguishi MS, Ribeiro AMA (2008) Detailed phenological scale of the reproductive phase of Coffea arabica Bragantia 67:257-260.
Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biology 10:142. doi: 10.1186/1471-2229-10-142
Peng Y, Lin W, Cai W, Aroca R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729-740.
Pinheiro HA, DaMatta FM, Chaves ARM, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora Annals of Botany 96:101-108.
Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schaeffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiology 152:1418-1430.
Rezaian MA, Krake LR (1987) Nucleic-acid extraction and virus detection in grapevine. Journal of Virological Methods 17:277-285
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.
Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant and Cell Physiology 46:1568-1577.
Santos AB, Mazzafera P (2012) Dehydrins are highly expressed in water-stressed plants of two coffee species. Tropical Plant Biology 5:218-232.
Schaffner AR (1998) Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204:131-139.
Shelden MC, Howitt SM, Kaiser BN, Tyerman SD (2009) Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera Functional Plant Biology 36:1065-1078.
Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869-876.
Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca Plant and Cell Physiology 42:686-693.
Smith AW (1989) Introduction. In Clarke RJ and Macrae R, editors. Coffee London: Elsevier. pp.1-41.
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596-1599.
Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22:4673-4680.
Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (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.
Vidal RO, Mondego JMC, Pot D, Ambrosio AB, Andrade AC, Pereira LF, Colombo CA, Vieira LGE, Carazzolle MF, Pereira GAG (2010) A high-throughput data mining of single nucleotide polymorphisms in coffea species expressed sequence tags suggests differential homeologous gene expression in the allotetraploid Coffea arabica Plant Physiology 154:1053-1066.
Vieira LGE, Andrade AC, Colombo CA, Moraes AHA et al. (2006) Brazilian coffee genome project: an EST-based genomic resource. Brazilian Journal Plant Physiology 18:95-108.
Wudick MM, Luu DT, Maurel C (2009) A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytologist 184:289-302.
Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biology of the Cell 97:397-414.
Zhang Y, Wang Z, Chai T, Wen Z, Zhang H (2008) Indian mustard aquaporin improves drought and heavy-metal resistance in tobacco. Molecular Biotechnology 40:280-292.

Publication Dates

Publication in this collection
15 Oct 2013
Date of issue
2013

History

Received
14 June 2013
Accepted
19 June 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Agre P, Sasaki, S, Chrispeels MJ (1993) Aquaporins: a family of water channel proteins. American Journal of Physiology - Renal Physiology 265:F461-F461.

[2] Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439-447.

[3] Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Molecular Biology 59:469-484.

[4] Aroca R, Ferrante A, Vernieri P, Chrispeels MJ (2006) Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Annals of Botany 98:1301-1310.

[5] Aroca R, Porcel R, Ruiz-Lozano MJ (2012) Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany 63:43-57.

[6] Baiges I, Schaffner AR, Mas A (2001) Eight cDNA encoding putative aquaporins in Vitis hybrid Richter-110 and their differential expression. Journal of Experimental Botany 52:1949-1951.

[7] Barsalobres-Cavallari CF, Severino FE, Maluf MP, Maia IG (2009) Identification of suitable internal control genes for expression studies in Coffea arabica under different experimental conditions. BMC Molecular Biology 10:1.

[8] Bogeat-Triboulot MB, Brosche M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman JF, Polle A, Kangasjärvi J, Dreyer E (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiology 143:876-892.

[9] Cenci A, Combes MC, Lashermes P (2010) Comparative sequence analyses indicate that Coffea (Asterids) and Vitis (Rosids) derive from the same paleo-hexaploid ancestral genome. Molecular Genetics and Genomics 283:493-501.

[10] Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiology 122:1025-1034.

[11] Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung, R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiology 125:1206-1215.

[12] DaMatta F, Ramalho J (2006) Impacts of drought and temperature stress on coffee physiology and production: a review. Brazilian Journal Plant Physiology 18:55-81.

[13] DaMatta FM, Chaves ARM, Pinheiro HA, Ducatti C, Loureiro ME (2003) Drought tolerance of two field-grown clones of Coffea canephora Plant Science 164:111-117.

[14] Danielson JAH, Johanson U (2008) Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens BMC Plant Biology 8:45.

[15] Dias PC, Araujo WL, Moraes GABK, Barros RS, DaMatta FM (2007) Morphological and physiological responses of two coffee progenies to soil water availability. Journal of Plant Physiology 164:1639-1647.

[16] Fahl JI, Carelli MLC, Gallo PB, Costa WM, Novo MCSS (1998) Enxertia de Coffea arabica sobre progênies de C. canephora e de C. congensis no crescimento, nutrição mineral e produção. Bragantia 52:297-312.

[17] Fahl JI, Carelli MLC, Menezes HC, Gallo PB Trivelin PCO (2001) Gas exchage, growth, yield and beverage quality of Coffea arabica cultivars grafted on to C. canephora and C. congensis Experimental Agriculture 37:241-252.

[18] Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215-228.

[19] Forrest KL, Bhave M (2008) The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Functional and Integrative Genomics 8:115-133.

[20] Galmes J, Pou A, Alsina MM, Tomas M, Medrano H, Flexas J (2007) Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta 226:671-681.

[21] Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu MH, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Research 16:277-286.

[22] Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: Characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biology 9:134. doi: 10.1186/1471-2229-9-134

[23] Guyot R, Lefebvre-Pautigny F, Tranchant-Dubreuil C, Rigoreau M, Hamon P, Leroy T, Hamon S, Poncet V, Crouzillat D, de Kochko A (2012) Ancestral synteny shared between distantly-related plant species from the asterid (Coffea canephora and Solanum sp.) and rosid (Vitis vinifera) clades. BMC Genomics 13: 103. doi: 10.1186/1471-2164-13-103.

[24] Hachez C, Heinen RB, 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.

[25] 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.

[26] Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, pp.95-98.

[27] Huang XQ (1992) A contig assembly program based on sensitive detection of fragment overlaps. Genomics 14:18-25.

[28] Jang JY, Kim DG, Kim YO, Kim JS, Kang HS (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana Plant Molecular Biology 54:713-725.

[29] Jang JY, Lee SH, Rhee JY, Chung GC, Ahn SJ, Kang H (2007a) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Molecular Biology 64:621-632.

[30] Jang JY, Rhee JY, Kim DG, Chung GC, Lee JH, Kang H (2007b) Ectopic expression of a foreign aquaporin disrupts the natural expression patterns of endogenous aquaporin genes and alters plant responses to different stress conditions. Plant and Cell Physiology 48:1331-1339.

[31] Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509-522.

[32] Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiology 126:1358-1369.

[33] 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. doi: 10.1111/j.1365-3040.2008.01792.x

[34] Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant and Cell Physiology 43:885-893.

[36] Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant and Cell Physiology 45:481-489.

[37] Lin CW, Mueller LA, McCarthy J, Crouzillat D, Petiard V, Tanksley SD (2005) Coffee and tomato share common gene repertoires as revealed by deep sequencing of seed and cherry transcripts. Theoretical and Applied Genetics 112:114-130.

[38] Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant, Cell and Environment 28:85-96.

[39] Mahdieh M, Mostajeran A, Horie T, Katsuhara M (2008) Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant and Cell Physiology 49:801-813.

[40] Manuel Ruiz-Lozano J, del Mar Alguacil M, Barzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Molecular Biology 70:565-579.

[41] Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology 130:2101-2110.

[42] Maurel C, Verdoucq L, Luu D-T, Santoni, V (2008) Plant aquaporins: Membrane channels with multiple integrated functions. Annual Review of Plant Biology 59:595-624.

[43] Mondego JMC, Vidal RO, Carazzolle MF, Tokuda EK, Parizzi LP, Costa GG, Pereira LF, Andrade AC, Colombo CA, Vieira LG, Pereira GA, Brazilian Coffee Genome Project Consortium (2011) An EST-based analysis identifies new genes and reveals distinctive gene expression features of Coffea arabica and Coffea canephora BMC Plant Biology 11:30. doi: 10.1186/1471-2229-11-30.

[44] Moraes MV, Franco CM (1973) Método expedito para enxertia em café. Instituto Brasileiro do Café, Rio de Janeiro. 8p.

[45] Morais H, Caramori PH, Koguishi MS, Ribeiro AMA (2008) Detailed phenological scale of the reproductive phase of Coffea arabica Bragantia 67:257-260.

[46] Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biology 10:142. doi: 10.1186/1471-2229-10-142

[47] Peng Y, Lin W, Cai W, Aroca R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729-740.

[48] Pinheiro HA, DaMatta FM, Chaves ARM, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora Annals of Botany 96:101-108.

[49] Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schaeffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiology 152:1418-1430.

[50] Rezaian MA, Krake LR (1987) Nucleic-acid extraction and virus detection in grapevine. Journal of Virological Methods 17:277-285

[51] 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.

[52] Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant and Cell Physiology 46:1568-1577.

[53] Santos AB, Mazzafera P (2012) Dehydrins are highly expressed in water-stressed plants of two coffee species. Tropical Plant Biology 5:218-232.

[54] Schaffner AR (1998) Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204:131-139.

[55] Shelden MC, Howitt SM, Kaiser BN, Tyerman SD (2009) Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera Functional Plant Biology 36:1065-1078.

[56] Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869-876.

[57] Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca Plant and Cell Physiology 42:686-693.

[58] Smith AW (1989) Introduction. In Clarke RJ and Macrae R, editors. Coffee London: Elsevier. pp.1-41.

[59] Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596-1599.

[60] Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22:4673-4680.

[61] Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (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.

[62] Vidal RO, Mondego JMC, Pot D, Ambrosio AB, Andrade AC, Pereira LF, Colombo CA, Vieira LGE, Carazzolle MF, Pereira GAG (2010) A high-throughput data mining of single nucleotide polymorphisms in coffea species expressed sequence tags suggests differential homeologous gene expression in the allotetraploid Coffea arabica Plant Physiology 154:1053-1066.

[63] Vieira LGE, Andrade AC, Colombo CA, Moraes AHA et al. (2006) Brazilian coffee genome project: an EST-based genomic resource. Brazilian Journal Plant Physiology 18:95-108.

[64] Wudick MM, Luu DT, Maurel C (2009) A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytologist 184:289-302.

[65] Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biology of the Cell 97:397-414.

[66] Zhang Y, Wang Z, Chai T, Wen Z, Zhang H (2008) Indian mustard aquaporin improves drought and heavy-metal resistance in tobacco. Molecular Biotechnology 40:280-292.

Brasil

Brasil

Aquaporins and the control of the water status in coffee plants

Abstract

Publication Dates

History