Enhancement of root hydraulic conductivity by methyl jasmonate and the role of calcium and abscisic acid in this process

Plant, Cell and Environment

Volumn 37, Issue 4, 2014, Pages 995-1008

  Sánchez Romera, Beatriz ^a   Ruiz Lozano, Juan Manuel ^a   Li, Guowei ^b   Luu, Doan Trung ^b   Martínez Ballesta, Maria Del Carmen ^c   Carvajal, Micaela ^c   Zamarreño, Angel María ^d   García Mina, Jose María ^d   Maurel, Christophe ^b   Aroca, Ricardo ^a  

^a CSIC   (Spain)

^b UNIV MONTPELLIER   (France)

^c RESEARCH GROUP ON QUALITY   (Spain)

^d CIPAV R and D Timac Agro Int (TAI) Roullier Group   (Spain)

Author keywords

Aquaporins; Arabidopsis thaliana; Phaseolus vulgaris; Solanum lycopersicum

Indexed keywords

ABSCISIC ACID; CALCIUM; DICOTYLEDON; FRUIT; HYDRAULIC CONDUCTIVITY; PHYTOCHEMISTRY; SIGNAL; STOMATAL CONDUCTANCE;

ARABIDOPSIS THALIANA; LYCOPERSICON ESCULENTUM; PHASEOLUS VULGARIS;

ABSCISIC ACID; ACETIC ACID DERIVATIVE; AQUAPORIN; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CHELATING AGENT; CYCLOPENTANE DERIVATIVE; HEPARIN; JASMONIC ACID METHYL ESTER; LANTHANUM; LANTHANUM CHLORIDE; OXYLIPIN; VEGETABLE PROTEIN; WATER;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHASEOLUS; PHASEOLUS VULGARIS; PHYSIOLOGY; PLANT ROOT; STAINING; TOMATO;

AQUAPORINS; ARABIDOPSIS THALIANA; PHASEOLUS VULGARIS; SOLANUM LYCOPERSICUM;

ABSCISIC ACID; ACETATES; ARABIDOPSIS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CHELATING AGENTS; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; HEPARIN; LANTHANUM; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; OXYLIPINS; PHASEOLUS; PLANT PROTEINS; PLANT ROOTS; STAINING AND LABELING; WATER;

EID: 84896696301     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12214     Document Type: Article

References (98)

1. Adie B.A.T., Perez-Perez J., Perez-Perez M.M., Godoy M., Sanchez-Serrano J.J., Schmelz E.A. & Solano R. (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. The Plant Cell 19, 1665-1681.
2. Akter N., Okuma E., Sobahan M.A., Uraji M., Munemasa S., Nakamura Y., ... Murata Y. (2013) Negative regulation of methyl jasmonate-induced stomatal closure by glutathione in Arabidopsis. Journal of Plant Growth Regulation 32, 208-215.
3. Amelot N., de Borne F.D., San Clemente H., Mazars C., Grima-Pettenati J. & Briere C. (2012) Transcriptome analysis of tobacco BY-2 cells elicited by cryptogein reveals new potential actors of calcium-dependent and calcium-independent plant defense pathways. Cell Calcium 51, 117-130.
4. Anjum S.A., Wang L., Farooq M., Khan I. & Xue L. (2011) Methyl jasmonate-induced alteration in lipid peroxidation, antioxidative defence system and yield in soybean under drought. Journal of Agronomy and Crop Science 197, 296-301.
5. Aroca R. (2006) Exogenous catalase and ascorbate modify the effects of abscisic acid (ABA) on root hydraulic properties in Phaseolus vulgaris L. plants. Journal of Plant Growth Regulation 25, 10-17.
6. Aroca R., Amodeo G., Fernandez-Illescas S., Herman E.M., Chaumont F. & Chrispeels M.J. (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiology 137, 341-353.
7. Aroca R., Ferrante A., Vernieri P. & Chrispeels M.J. (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.
8. Aroca R., Porcel R. & Ruiz-Lozano J.M. (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytologist 173, 808-816.
9. Aroca R., Vernieri P. & Ruiz-Lozano J.M. (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Botany 59, 2029-2041.
10. Aroca R., Porcel R. & Ruiz-Lozano J.M. (2012) Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany 63, 43-57.
11. Aroca R., Ruiz-Lozano J.M., Zamarreno A.M., Paz J.A., Garcia-Mina J.M., Pozo M.J. & Lopez-Raez J.A. (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. Journal of Plant Physiology 170, 47-55.
12. Azad A.K., Katsuhara M., Sawa Y., Ishikawa T. & Shibata H. (2008) Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation. Plant and Cell Physiology 49, 1196-1208.
13. Beaudette P.C., Chlup M., Yee J. & Emery R.J.N. (2007) Relationships of root conductivity and aquaporin gene expression in Pisum sativum: diurnal patterns and the response to HgCl2 and ABA. Journal of Experimental Botany 58, 1291-1300.
14. Benabdellah K., Ruiz-Lozano J.M. & Aroca R. (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Molecular Biology 70, 647-661.
15. Boter M., Ruiz-Rivero O., Abdeen A. & Prat S. (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes & Development 18, 1577-1591.
16. Boursiac Y., Chen S., Luu D.T., Sorieul M., van den Dries N. & Maurel C. (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiology 139, 790-805.
17. Boursiac Y., Boudet J., Postaire O., Luu D.T., Tournaire-Roux C. & Maurel C. (2008) Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. The Plant Journal 56, 207-218.
18. Bradford M.M. & Williams W.L. (1976) New, rapid, sensitive method for protein determination. Federation Proceedings 35, 274-274.
19. Chae S.H., Yoneyama K., Takeuchi Y. & Joel D.M. (2004) Fluridone and norflurazon, carotenoid-biosynthesis inhibitors, promote seed conditioning and germination of the holoparasite Orobanche minor. Physiologia Plantarum 120, 328-337.
20. 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.
21. 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.
22. Cutler S.R., Ehrhardt D.W., Griffitts J.S. & Somerville C.R. (2000) Random GFP: cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proceedings of the National Academy of Sciences of the United States of America 97, 3718-3723.
23. Farmer E.E., Almeras E. & Krishnamurthy V. (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology 6, 372-378.
24. 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.
25. Fiscus E.L. (1986) Diurnal cahnges in volume and solute transport coefficients of Phaeolus roots. Plant Physiology 80, 752-759.
26. Fonseca S., Chini A., Hamberg M., Adie B., Porzel A., Kramell R., ... Solano R. (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5, 344-350.
27. Gehring C.A., Irving H.R., McConchie R. & Parish R.W. (1997) Jasmonates induce intracellular alkalinization and closure of Paphiopedilum guard cells. Annals of Botany 80, 485-489.
28. Gerbeau P., Amodeo G., Henzler T., Santoni V., Ripoche P. & Maurel C. (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. The Plant Journal 30, 71-81.
29. Gould N., Reglinski T., Northcott G.L., Spiers M. & Taylor J.T. (2009) Physiological and biochemical responses in Pinus radiata seedlings associated with methyl jasmonate-induced resistance to Diplodia pinea. Physiological and Molecular Plant Pathology 74, 121-128.
30. 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.
31. Herde O., Pena Cortes H., Willmitzer L. & Fisahn J. (1997) Stomatal responses to jasmonic acid, linolenic acid and abscisic acid in wild-type and ABA-deficient tomato plants. Plant, Cell & Environment 20, 136-141.
32. Hossain M.A., Munemasa S., Uraji M., Nakamura Y., Mori I.C. & Murata Y. (2011) Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis. Plant Physiology 156, 430-438.
33. Howe G.A. & Ryan C.A. (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153, 1411-1421.
34. Howe G.A., Lightner J., Browse J. & Ryan C.A. (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in siganling for defense against insect attack. The Plant Cell 8, 2067-2077.
35. Islam M.M., Hossain M.A., Jannat R., Munemasa S., Nakamura Y., Mori I.C. & Murata Y. (2010) Cytosolic alkalization and cytosolic calcium oscillation in Arabidopsis guard cells response to ABA and MeJA. Plant and Cell Physiology 51, 1721-1730.
36. Javot H., Lauvergeat V., Santoni V., Martin-Laurent F., Guclu J., Vinh J., ... Maurel C. (2003) Role of a single aquaporin isoform in root water uptake. The Plant Cell 15, 509-522.
37. Johanson U., Karlsson M., Johansson I., Gustavsson S., Sjovall S., Fraysse L., ... Kjellbom P. (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis. Plant Physiology 126, 1358-1369.
38. Johansson I., Karlsson M., Shukla V.K., Chrispeels M.J., Larsson C. & Kjellbom P. (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. The Plant Cell 10, 451-459.
39. Johansson I., Karlsson M., Johanson U., Larsson C. & Kjellbom P. (2000) The role of aquaporins in cellular and whole plant water balance. Biochimica et Biophysica Acta 1465, 324-342.
40. Kay R., Chan A., Daly M. & McPherson J. (1987) Duplication of CAMV-35S promoter sequences creates a strong enhancer for plant genes. Science 236, 1299-1302.
41. Kim H.J., Fonseca J.M., Choi J.H. & Kubota C. (2007) Effcet of methyl jasmonate on phenolic compounds and carotenoids of romaine lettuce (Lactuca sativa L.). Journal of Agriculture and Food Chemistry 55, 10366-10372.
42. Klaas M., Yang B., Bosch M., Thorogood D., Manzanares C., Armstead I.P., ... Barth S. (2011) Progress towards elucidating the mechanisms of self-incompatibility in the grasses: further insights from studies in Lolium. Annals of Botany 108, 677-685.
43. Kramell R., Atzorn R., Schneider G., Miersch O., Bruckner C., Schmidt J., ... Parthier B. (1995) Occurrence and identification of jasmonic acid and its amino-acid conjugates induced by osmotic-stress in barley leaf tissue. Journal of Plant Growth Regulation 14, 29-36.
44. Kudoyarova G., Veselova S., Hartung W., Farhutdinov R., Veselov D. & Sharipova G. (2011) Involvement of root ABA and hydraulic conductivity in the control of water relations in wheat plants exposed to increased evaporative demand. Planta 233, 87-94.
45. Lee T.M., Lur H.S., Lin Y.H. & Chu C. (1996) Physiological and biochemical changes related to methyl jasmonate-induced chilling tolerance of rice (Oryza sativa L) seedlings. Plant, Cell & Environment 19, 65-74.
46. Li C.Y., Williams M.M., Loh Y.T., Lee G.I. & Howe G.A. (2002) Resistance of cultivated tomato to cell conetnt-feeding herbivores is regulated by octadecanoid-signaling pathway. Plant Physiology 130, 494-503.
47. Li D.D., Ruan X.M., Zhang J., Wu Y.J., Wang X.L. & Li X.B. (2013) Cotton plasma membrane intrinsic protein 2s (PIP2s) selectively intearct to regulate their water channel activities and are required for fibre development. New Phytologist 199, 695-707.
48. 2+ and calmodulin. Plant Science 185, 185-189.
49. Livak K.J. & Schmittgen T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402-408.
50. López-Ráez J.A., Verhage A., Fernández I., García J.M., Azcón-Aguilar C., Flors V. & Pozo M.J. (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. Journal of Experimental Botany 61, 2589-2601.
51. Lorenzo O. & Solano R. (2005) Molecular players regulating the jasmonate signalling network. Current Opinion in Plant Biology 8, 532-540.
52. Mahdieh M. & Mostajeran A. (2009) Abscisic acid regulates root hydraulic conductance via aquaporin expression modulation in Nicotiana tabacum. Journal of Plant Physiology 166, 1993-2003.
53. Marulanda A., Azcon R., Chaumont F., Ruiz-Lozano J.M. & Aroca R. (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232, 533-543.
54. Maurel C., Kado R.T., Guern J. & Chrispeels M.J. (1995) Phosphorylation regulates the water channel activity of the seed- specific aquaporin alpha-TIP. EMBO Journal 14, 3028-3035.
55. 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.
56. Munemasa S., Oda K., Watanabe-Sugimoto M., Nakamura Y., Shimoishi Y. & Murata Y. (2007) The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiology 143, 1398-1407.
57. Munemasa S., Hossain M.A., Nakamura Y., Mori I.C. & Murata Y. (2011) The Arabidopsis calcium-dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiology 155, 553-561.
58. Nagel O.W., Konings H. & Lambers H. (1994) Growth-rate, plant development and water relations of the ABA-deficient tomato mutant sitiens. Physiologia Plantarum 92, 102-108.
59. O'Donnell P.J., Schmels E., Block A., Miersch O., Wasternack C., Jones J.B. & Klee H.J. (2003) Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiology 133, 1181-1189.
60. 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.
61. Pauwels L., Morreel K., De Witte E., Lammertyn F., Van Montagu M., Boerjan W., ... Goossens A. (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and. Proceedings of the National Academy of Sciences of the United States of America 105, 1380-1385.
62. Peret B., Li G., Zhao J., Band L.R., Voss U., Postaire O., ... Bennett M.J. (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology 14, 991-1006.
63. Perrone I., Gambino G., Chitarra W., Vitali M., Pagliarani C., Riccomagno N., ... Lovisolo C. (2012) The grapevine root-specific aquaporin VvPIP2;4N controls root hydraulic conductance and leaf gas exchange under well-watered conditions but not under water stress. Plant Physiology 160, 965-977.
64. Porcel R., Aroca R., Azcon R. & Ruiz-Lozano J.M. (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Molecular Biology 60, 389-404.
65. Postaire O., Tournaire-Roux C., Grondin A., Boursiac Y., Morillon R., Schaffner A.R. & 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.
66. 2+-release components act in opposite ways in the regulation of the auxin-dependent MIA biosynthesis in Catharanthus roseus cells. Journal of Experimental Botany 60, 1387-1398.
67. Prak S., Hem S., Boudet J., Viennois G., Sommerer N., Rossignol M., ... Santoni V. (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins. Molecular & Cellular Proteomics 7, 1019-1030.
68. Raghavendra A.S. & Reddy K.B. (1987) Action of proline on stomata differs from that of abscisic acid, g-substances, or methyl jasmonate. Plant Physiology 83, 732-734.
69. Reddy A.S.N., Ali G.S., Celesnik H. & Day I.S. (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. The Plant Cell 23, 2010-2032.
70. Ruiz-Lozano J.M., Alguacil M.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.
71. Sade N., Vinocur B.J., Diber A., Shatil A., Ronen G., Nissan H., ... Moshelion M. (2009) Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytologist 181, 651-661.
72. 2+ signals: the versatile decoders of environmental cues. Critical Reviews in Biotechnology 33, 97-109.
73. 2. Plant Physiology 87, 583-587.
74. Secchi F., Perrone I., Chitarra W., Zwieniecka A.K., Lovisolo C., & Zwieniecki M.A. (2013) The dynamics of embolism refilling in abscisic acid (ABA)-deficient tomato plants. International Journal of Molecular Sciences 14, 359-377.
75. Steudle E. (1997) Water transport across plant tissue: role of water channels. Biology of the Cell 89, 259-273.
76. Steudle E. & Peterson C.A. (1998) How does water get through roots? Journal of Experimental Botany 49, 775-788.
77. Suhita D., Raghavendra A.S., Kwak J.M. & Vavasseur A. (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiology 134, 1536-1545.
78. Sun J., Cardoza V., Mitchell D.M., Bright L., Oldroyd G. & Harris J.M. (2006a) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. The Plant Journal 46, 961-970.
79. 2+]cyt and JR1 expression in Arabidopsis thaliana. Journal of Plant Research 119, 343-350.
80. Sun Q.P., Yu Y.K., Wan S.X., Zhao F.K. & Hao Y.L. (2009) Is there crosstalk between extracellular and intracellular calcium mobilization in jasmonic acid signaling. Plant Growth Regulation 57, 7-13.
81. Sutka M., Li G., Boudet J., Boursiac Y., Doumas P. & Maurel C. (2011) Natural variation of root hydraulics in Arabidopsis grown in normal and salt-stressed conditions. Plant Physiology 155, 1264-1276.
82. Taylor I.B., Linforth R.S.T., Alnaieb R.J., Bowman W.R. & Marples B.A. (1988) The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA- aldehyde to ABA. Plant, Cell & Environment 11, 739-745.
83. Tester M. & Macrobbie E.A.C. (1990) Cytoplasmic calcium affects the gating of potassium channel in the plasma-membrane of Chara corallina a whole-cell study using calcium-channel effectors. Planta 180, 569-581.
84. Thompson A.J., Andrews J., Mulholland B.J., McKee J.M.T., Hilton H.W., Horridge J.S., ... Taylor I.B. (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiology 143, 1905-1917.
85. Törnroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., ... Kjellbom P. (2006) Structural mechanism of plant aquaporin gating. Nature 439, 688-694.
86. Tournaire-Roux C., Sutka M., Javot H., Gout E., Gerbeau P., Luu D.T., ... Maurel C. (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393-397.
87. Wang P. & Song C.P. (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytologist 178, 703-718.
88. Wasternack C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant. Annals of Botany 100, 681-697.
89. Wasternack C. & Hause B. (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111, 1021-1058.
90. Wen K., Seguin P.S., Arnaud M. & Jabaji-Hare S. (2005) Real-time quantitative RT-PCR of defense-associated gene transcripts of Rhizoctonia solani-infected bean seedlings in response to inoculation with a nonpathogenic binucleate Rhizoctonia isolate. Phytopathology 95, 345-353.
91. White P.J. (2000) Calcium channels in higher plants. Biochimica et Biophysica Acta 1465, 171-189.
92. Wu H., Wu X., Li Z., Duan L. & Zhang M. (2012a) Physiological evaluation of drought stress tolerance and recovery in cauliflower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. Journal of Plant Growth Regulation 31, 113-123.
93. Wu Y., Liu X., Wang W., Zhang S. & Xu B. (2012b) Calcium regulates the cell-to-cell water flow pathway in maize roots during variable water conditions. Plant Physiology and Biochemistry 58, 212-219.
94. 2+ release from skinned rat aortic smooth-muscle cells in primary culture. Naunyn-Schmiedebergs Archives of Pharmacology 341, 273-278.
95. Yang Y., Yang F., Li X., Shi R. & Lu J. (2013) Signal regulation of proline metabolism in callus of the halophyte Nitraria tangutorum Bobr. grown under salinity stress. Plant Cell Tissue and Organ Culture 112, 33-42.
96. Yu M., Shen L., Zhang A. & Sheng J. (2011) Methyl jasmonate-induced defense responses are associated with elevation of 1-aminocyclopropane-1-carboxy oxidase in Lycopersicon esculentum fruit. Journal of Plant Physiology 168, 1820-1827.
97. 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.
98. Zhou Y., Setz N., Niemietz C., Qu H., Offler C.E., Tyerman S.D. & Patrick J.W. (2007) Aquaporins and unloading of phloem-imported water in coats of developing bean seeds. Plant, Cell & Environment 30, 1566-1577.