β-amylase1 mutant Arabidopsis plants show improved drought tolerance due to reduced starch breakdown in guard cells

Journal of Experimental Botany

Volumn 66, Issue 19, 2015, Pages 6059-6067

  Prasch, Christian Maximilian ^a   Ott, Kirsten Verena ^a   Bauer, Hubert ^b   Ache, Peter ^b   Hedrich, Rainer ^b   Sonnewald, Uwe ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Arabidopsis; Drought; Guard cells; Starch; amylases

Indexed keywords

ARABIDOPSIS PROTEIN; BAM1 PROTEIN, ARABIDOPSIS; PROTEIN SERINE THREONINE KINASE; STARCH; WATER;

ARABIDOPSIS; DOWN REGULATION; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DOWN-REGULATION; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; PROTEIN-SERINE-THREONINE KINASES; STARCH; STRESS, PHYSIOLOGICAL; WATER;

EID: 84942274797     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv323     Document Type: Article

References (49)

1. Antunes WC, Provart NJ, Williams TC, Loureiro ME. 2012. Changes in stomatal function and water use efficiency in potato plants with altered sucrolytic activity. Plant Cell & Environment 35, 747-759.
2. Bauer H, Ache P, Wohlfart F, Al-Rasheid KA, Sonnewald S, Sonnewald U, Kneitz S, Hetherington AM, Hedrich R. 2013. How do stomata sense reductions in atmospheric relative humidity? Molecular Plant 6, 1703-1706.
3. Biemelt S, Tschiersch H, Sonnewald U. 2004. Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiology 135, 254-265.
4. Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E. 2006. Integration of abscisic acid signalling into plant responses. Plant Biology 8, 314-325.
5. Daszkowska-Golec A, Szarejko I. 2013. Open or close the gate-stomata action under the control of phytohormones in drought stress conditions. Frontiers in Plant Science 4, 138.
6. Datta R, Selvi M, Seetharama N, Sharma R. 1999. Stress-mediated enhancement of ß-amylase activity in pearl millet and maize leaves is dependent on light. Plant Physiology and Biochemistry 154, 657-664.
7. Dreier W, Schnarrenberger C, Borner T. 1995. Light-and stressdependent enhancement of amylolytic activities in white and green barley leaves: beta-amylases are stressinduced proteins. Plant Physiology 145, 342-348.
8. Edwards K, Johnstone C, Thompson C. 1991. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Research 19, 1349.
9. FAO. 2014. http://www. fao. org/nr/water/aquastat/water-use/index. stm.
10. Finkelstein RR, Gibson SI. 2002. ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Current Opinion in Plant Biology 5, 26-32.
11. Fulton DC, Stettler M, Mettler T, et al. 2008. Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. The Plant Cell 20, 1040-1058.
12. Geiger D, Scherzer S, Mumm P, et al. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinasephosphatase pair. Proceedings of the National Academy of Sciences of the United States of America 106, 21425-21430.
13. Goujon T, Minic Z, El Amrani A, Lerouxel O, Aletti E, Lapierre C, Joseleau JP, Jouanin L. 2003. AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. The Plant Journal 33, 677-690.
14. Hedrich R. 2012. Ion channels in plants. Physiological Reviews 92, 1777-1811.
15. Jones L, Milne JL, Ashford D, McQueen-Mason SJ. 2003. Cell wall arabinan is essential for guard cell function. Proceedings of the National Academy of Sciences of the United States of America 100, 11783-11788.
16. Kaplan F, Guy CL. 2004. beta-Amylase induction and the protective role of maltose during temperature shock. Plant Physiology 135, 1674-1684.
17. Kaplan F, Guy CL. 2005. RNA interference of Arabidopsis ß-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. The Plant Journal 44, 730-743.
18. Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R, Attia Z, Belausov E, Granot D. 2013. Hexokinase mediates stomatal closure. The Plant Journal 75, 977-988.
19. Laluk K, Abuqamar S, Mengiste T. 2011. The Arabidopsis mitochondria-localized pentatricopeptide repeat protein PGN functions in defense against necrotrophic fungi and abiotic stress tolerance. Plant Physiology 156, 2053-2068.
20. Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA. 1999. An Arabidopsis gene encoding a chloroplast-targeted betaamylase. The Plant Journal 20, 519-527.
21. Lawson T, Lefebvre S, Baker NR, Morison JI, Raines CA. 2009. Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2. Journal of Experimental Botany 59, 3609-3619.
22. Lawson T, Blatt MR. 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiology 164, 1556-1570.
23. 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. The Cell 126, 1109-1120.
24. Logemann J, Schell J, Willmitzer L. 1987. Improved method for the isolation of RNA from plant tissues. Analytical Biochemistry 163, 16-20.
25. Maeo K, Tomiya T, Hayashi K, Akaike M, Morikami A, Ishiguro S, Nakamura K. 2001. Sugar-responsible elements in the promoter of a gene for beta-amylase of sweet potato. Plant Molecular Biology 46, 627-637.
26. Maruyama K, Takeda M, Kidokoro S, et al. 2009. Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiology 150, 1972-1980.
27. Mita S, Suzuki-Fujii K, Nakamura K. 1995. Sugar-inducible expression of a gene for beta-amylase in Arabidopsis thaliana. Plant Physiology 107, 895-904.
28. Mizoguchi M, Umezawa T, Nakashima K, Kidokoro S, Takasaki H, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K. 2010. Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant and Cell Physiology 51, 842-847.
29. Monroe JD, Storm AR, Badley EM, Lehman MD, Platt SM, Saunders LK, Schmitz JM, Torres CE. 2014. beta-Amylase1 and beta-amylase3 are plastidic starch hydrolases in Arabidopsis that seem to be adapted for different thermal, pH, and stress conditions. Plant Physiology 166, 1748-1763.
30. Nakashima K, Ito Y, Yamaguchi-Shinozaki K. 2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiology 149, 88-95.
31. Outlaw WH, Manchester J. 1979. Guard cell starch concentration quantitatively related to stomatal aperture. Plant Physiology 64, 79-82.
32. Overlach S, Diekmann W, Raschke K. 1993. Phosphate Translocator of Isolated Guard-Cell Chloroplasts from Pisum sativum L. Transports Glucose-6-Phosphate. Plant Physiology 101, 1201-1207.
33. Prasch CM, Sonnewald U. 2013. Simultaneous application of heat, drought and virus to Arabidopsis thaliana plants reveals significant shifts in signaling networks. Plant Physiology 162, 1849-1866.
34. Raghavendra AS, Gonugunta VK, Christmann A, Grill E. 2010. ABA perception and signalling. Trends Plant Science 15, 395-401.
35. Raschke K, Hedrich R. 1985. Simultaneous and independent effects of abscisic acid on stomata and the photosynthetic apparatus in whole leaves. Planta 163, 105-118.
36. Roelfsema MR, Hedrich R, Geiger D. 2012. Anion channels: master switches of stress responses. Trends in Plant Science 17, 221-229.
37. Schmitz-Linneweber C, Small I. 2008. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends in Plant Science 13, 663-670.
38. Schnabl H. 1980. CO2 and malate metabolism in starch-containing and starch-lacking guard-cell protoplast. Planta 14, 52-58.
39. Seifert GJ, Roberts K. 2007. The biology of arabinogalactan proteins. Annual Review of Plant Biology 58, 137-161.
40. Sicher R. 2011. Carbon partitioning and the impact of starch deficiency on the initial response of Arabidopsis to chilling temperatures. Plant Science 181, 167-176.
41. Sparla F, Costa A, Lo Schiavo F, Pupillo P, Trost P. 2006. Redox regulation of a novel plastid-targeted beta-amylase of Arabidopsis. Plant Physiology 141, 840-850.
42. Stitt M, Lilley RM, Gerhardt R, Heldt H-W. 1989. Determination of metabolite levels in specific cells and subcellular compartments of plant leaves. Methods in Enzymology 174, 518-522.
43. Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH. 2001. Multiple transcription-factor genes are early targets of phytochrome A signaling. Proceedings of the National Academy of Sciences of the United States of America 98, 9437-9442.
44. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914-939.
45. Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, Sparla F. 2011. Thioredoxin-regulated beta-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. Journal of Experimental Botany 62, 545-555.
46. Vissenberg K, Fry SC, Pauly M, Hofte H, Verbelen JP. 2005. XTH acts at the microfibril-matrix interface during cell elongation. Journal of Experimental Botany 56, 673-683.
47. Wang SM, Lue WL, Eimert K, Chen J. 1996. Phytohormone-regulated beta-amylase gene expression in rice. Plant Molecular Biology 31, 975-982.
48. Weise SE, Kim KS, Stewart RP, Sharkey TD. 2005. beta-Maltose is the metabolically active anomer of maltose during transitory starch degradation. Plant Physiology 137, 756-761.
49. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781-803.