Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots

Journal of Experimental Botany

Volumn 61, Issue 12, 2010, Pages 3395-3405

  Ernst, Laura ^a   Goodger, Jason Q D ^b   Alvarez, Sophie ^a   Marsh, Ellen L ^a   Berla, Bert ^a   Lockhart, Eric ^a   Jung, Jiyul ^a   Li, Pinghua ^c   Bohnert, Hans J ^c   Schachtman, Daniel P ^a  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

ABA biosynthesis; Abscisic acid; Corn; Drought; pH; Stomatal conductance; Sulphate; Water stress; Zea mays

Indexed keywords

ABSCISIC ACID; PLANT RNA; SULFATE; WATER; SOIL;

ARTICLE; BIOSYNTHESIS; CHEMISTRY; DEHYDRATION; ENZYMOLOGY; EVAPOTRANSPIRATION; GENETICS; MAIZE; METABOLISM; PLANT LEAF; PLANT ROOT; SIGNAL TRANSDUCTION; SOIL; TRANSPORT AT THE CELLULAR LEVEL; XYLEM; ANALYSIS;

ABSCISIC ACID; BIOLOGICAL TRANSPORT; DEHYDRATION; PLANT LEAVES; PLANT ROOTS; PLANT TRANSPIRATION; RNA, PLANT; SIGNAL TRANSDUCTION; SOIL; SULFATES; WATER; XYLEM; ZEA MAYS;

VICIA FABA; ZEA MAYS;

EID: 77954810665     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq160     Document Type: Article

References (66)

1. Alvarez S, Goodger JQD, Marsh EL, Chen SX, Asirvatham VS, Schachtman DP. 2006. Characterization of the maize xylem sap proteome. Journal of Proteome Research 5, 963-972.
2. Alvarez S, Marsh EL, Schroeder SG, Schachtman DP. 2008. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant, Cell and Environment 31, 325-340.
3. Assmann SM, Shimazaki KI. 1999. The multisensory guard cell. Stomatal responses to blue light and abscisic acid. Plant Physiology 119, 337-361.
4. Bacon MA, Wilkinson S, Davies WJ. 1998. pH-regulated leaf cell expansion in droughted plants is abscisic acid dependent. Plant Physiology 118, 1507-1515.
5. Blatt MR. 2000. Cellular signalling and volume control in stomatal movements in plants. Annual Review of Cellular and Developmental Biology 16, 221-241.
6. Borel C, Frey A, Marion-Poll A, Tardieu F, Simonneau T. 2001. Does engineering abscisic acid biosynthesis in Nicotiana plumbaginifolia modify stomatal response to drought? Plant, Cell and Environment 24, 477-489.
7. Buckley TN. 2005. The control of stomata by water balance. New Phytologist 168, 275-292.
8. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J. 2008. Identification and characterization of small RNAs from the phloem of Brassica napus. The Plant Journal 53, 739-749.
9. Cheng WH, Endo A, Zhou L, et al. 2002. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signalling and abscisic acid biosynthesis and functions. Plant, Cell and Environment 14, 2723-2743.
10. Christmann A, Hoffmann T, Teplova I, Grill E, Muller A. 2005. Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiology 137, 209-219.
11. Christmann A, Weiler EW, Steudle E, Grill E. 2007. A hydraulic signal in root-to-shoot signalling of water shortage. The Plant Journal 52, 167-174.
12. Cramer GR, Ergül A, Grimplet J, et al. 2007. Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Functional and Integrative Genomics 7, 111-134.
13. Davies WJ, Bacon MA, Thompson SD, Sobeih W, Rodr?́guez LG. 2000. Regulation of leaf and fruit growth in plants growing in drying soil: exploitation of the plants' chemical signalling system and hydraulic architecture to increase the efficiency of water use in agriculture. Journal of Experimental Botany 51, 1617-1626.
14. Davies WJ, Kudoyarova G, Hartung W. 2005. Long-distance ABA signalling and its relation to other signalling pathways in the detection of soil drying and the mediation of the plant's response to drought. Journal of Plant Growth Regulation 24, 285-295.
15. Davies WJ, Wilkinson S, Loveys BR. 2002. Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytologist 153, 449-460.
16. Dietz KJ, Sauter A, Wichert K, Messdaghi D, Hartung W. 2000. Extracellular beta-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. Journal of Experimental Botany 51, 937-944.
17. Endo A, Sawada Y, Takahashi H, et al. 2008. Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiology 147, 1984-1993.
18. Fambrini M, Vernieri P, Toncelli ML, Rossi VD, Pugliesi C. 1995. Characterisation of a wilty sunflower (Helianthus annuus L.) mutant. III. Phenotypic interaction in reciprocal grafts from wilty mutant and wild-type plants. Journal of Experimental Botany 46, 525-530.
19. Freundl E, Steudle E, Hartung W. 2000. Apoplastic transport of abscisic acid through roots of maize: effect of the exodermis. Planta 210, 222-231.
20. Gollan T, Passioura JB, Munns R. 1986. Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves. Australian Journal of Plant Physiology 13, 459-464.
21. Goodger JQD, Sharp RE, Marsh EL, Schachtman DP. 2005. Relationships between xylem sap constituents and leaf conductance of well-watered and water-stressed maize across three xylem sap sampling techniques. Journal of Experimental Botany 56, 2389-2400.
22. Hawkesford MJ. 2003. Transporter gene families in plants: the sulphate transporter gene family\redundancy or specialization? Physiologia Plantarum 117, 155-163.
23. Holbrook NM, Shashidhar VR, James RA, Munns R. 2002. Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. Journal of Experimental Botany 53, 1503-1514.
24. Ikegami K, Okamoto M, Seo M, Koshiba T. 2009. Activation of abscisic acid biosynthesis in the leaves of Arabidopsis thaliana in response to water deficit. Journal of Plant Research 122, 235-243.
25. Jackson MB. 1997. Hormones from roots as signals for the shoots of stressed plants. Trends in Plant Science 2, 22-28.
26. Jia W, Liang J, Zhang J. 2001. Initiation and regulation of water deficit-induced abscisic acid accumulation in maize leaves and roots: cellular volume and water relations. Journal of Experimental Botany 52, 295-300.
27. Jones HG, Sharp CS, Higgs KH. 1987. Growth and water relations of wilty mutants of tomato (Lycopersicon esculentum Mill.). Journal of Experimental Botany 38, 1848-1856.
28. Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T. 2004. Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiology 134, 1697-1707.
29. 2 fumigation and the participation of abscisic acid. Plant and Cell Physiology 19, 365-373.
30. Lawson T. 2009. Guard cell photosynthesis and stomatal function. New Phytologist 181, 13-34.
31. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ. 2006. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109-1120.
32. Li S, Assmann SM, Albert R. 2006. Predicting essential components of signal transduction networks: A dynamic model of guard cell abscisic acid signalling. PLoS Biology 4, e312: 1732-1748.
33. Liang J, Zhang J. 1997. Collection of xylem sap at flow rate similar to in vivo transpiration flux. Plant and Cell Physiology 38, 1375-1381.
34. Lü B, Chen F, Gong ZH, Xie H, Zhang JH, Liang JS. 2007. Intracellular localization of integrin-like protein and its roles in osmotic stress-induced abscisic acid biosynthesis in Zea mays. Protoplasma 232, 35-43.
35. Mahouachi J, Arbona V, Gó mez-Cadenas A. 2007. Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regulation 53, 43-51.
36. Munns R, King RW. 1988. Abscisic acid is not the only stomatal inhibitor in the transpiration stream of wheat plants. Plant Physiology 88, 703-708.
37. Neumann PM. 2007. Evidence for long-distance xylem transport of signal peptide activity from tomato roots. Journal of Experimental Botany 58, 2217-2223.
38. Neumann PM. 2008. Coping mechanisms for crop plants in drought-prone environments. Annals of Botany 101, 901-907.
39. Ng CKY, McAinsh MR, Gray JE, Hunt L, Leckie CP, Mills L, Hetherington AM. 2001. Calcium-based signalling systems in guard cells. New Phytologist 151, 109-120.
40. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, 2002-2007.
41. Priest DM, Ambrose SJ, Vaistij FE, Elias L, Higgins GS, Ross AR, Abrams SR, Bowles DJ. 2006. Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. The Plant Journal 46, 492-502.
42. Qin X, Zeevaart JAD. 1999. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proceedings of the National Academy of Sciences, USA 96, 15354-15361.
43. Reinoso H, Sosa L, Reginato M, Luna V. 2005. Histological alterations induced by sodium sulphate in the vegetative anatomy of Prosopis strombulifera (Lam.) Benth. World Journal of Agricultural Sciences 1, 109-119.
44. Rennenberg H. 1984. The fate of excess sulphur in higher plants. Annual Review of Plant Physiology 35, 121-153.
45. Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57, 431-449.
46. Sauter A, Davies WJ, Hartung W. 2001. The long-distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot. Journal of Experimental Botany 52, 1991-1997.
47. Sauter A, Hartung W. 2000. Radial transport of abscisic acid conjugates in maize roots: its implication for long distance stress signals. Journal of Experimental Botany 51, 929-935.
48. Sauter A, Hartung W. 2002. The contribution of internode and mesocotyl tissues to root-to-shoot signalling of abscisic acid. Journal of Experimental Botany 53, 297-302. (Pubitemid 34140376)
49. Schachtman DP, Goodger JQD. 2008. Chemical root to shoot signalling under drought. Trends in Plant Science 13, 281-287.
50. Schachtman DP, Shin R. 2007. Nutrient sensing and signalling: NPKS. Annual Review of Plant Biology 58, 47-69.
51. Schraut D, Heilmeier H, Hartung W. 2005. Radial transport of water and abscisic acid (ABA) in roots of Zea mays under conditions of nutrient deficiency. Journal of Experimental Botany 56, 879-886.
52. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D. 2001. Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 52, 627-658. (Pubitemid 33720050)
53. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yomeyama T, Davis JP. 2002. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulphate transporter required for efficient transport of sulphate into roots. The Plant Journal 29, 475-486.
54. Taylor JS, Reid DM, Pharis RP. 1981. Mutual antagonism of sulphur dioxide and abscisic acid in their effect on stomatal aperture in broad bean (Vicia faba L.) epidermal strips. Plant Physiology 68, 1504-1507.
55. Thompson AJ, Mulholland BJ, Jackson AC, McKee JMT, Hilton HW, Symonds RC, Sonneveld T, Burbidge A, Stevenson P, Taylor IB. 2007. Regulation and manipulation of ABA biosynthesis in roots. Plant, Cell and Environment 30, 67-78.
56. Wilkinson S. 1999. pH as a stress signal. Plant Growth Regulation 29, 87-99.
57. Wilkinson S, Bacon MA, Davies WJ. 2007. Nitrate signalling to stomata and growing leaves: interactions with soil drying, ABA, and xylem sap pH in maize. Journal of Experimental Botany 58, 1705-1716.
58. Wilkinson S, Corlett JE, Oger L. 1998. Effects of xylem pH on transpiration from wild-type and flacca tomato leaves: a vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiology 117, 703-709.
59. Wilkinson S, Davies WJ. 1997. Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiology 113, 559-573.
60. Wilkinson S, Davies WJ. 2002. ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant, Cell and Environment 25, 195-210.
61. Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. 2002. Two distinct high-affinity sulphate transporters with different inducibilities mediate uptake of sulphate in Arabidopsis roots. The Plant Journal 29, 465-473.
62. Zhang J, Schurr U, Davies WJ. 1987. Control of stomatal behaviour by abscisic acid which apparently originates in the roots. Journal of Experimental Botany 38, 1174-1181.
63. Zhang J, Tardieu F. 1996. Relative contribution of apices and mature tissues to ABA synthesis in droughted maize root systems. Plant and Cell Physiology 37, 598-605.
64. Zhang JH, Jia WS, Yang JC. 2004. ABA in plant water stress signalling. Proceedings of the Indian National Science Academy 70, 1-10.
65. Zhang MW, Davies WJ. 1990. Changes in the concentration of ABA in xylem sap as a function of changing soil water status can account for changes in leaf conductance and growth. Plant, Cell and Environment 13, 277-285.
66. Zhu JM, Alvarez S, Marsh EL, et al. 2007. Cell wall Proteome in the maize primary root elongation zone. II. Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiology 145, 1533-1548.