Wheat flag leaf epicuticular wax morphology and composition in response to moderate drought stress are revealed by SEM, FTIR-ATR and synchrotron X-ray spectroscopy

Physiologia Plantarum

Volumn 162, Issue 3, 2018, Pages 316-332

  Willick, Ian R ^a   Lahlali, Rachid ^b   Vijayan, Perumal ^a   Muir, David ^b   Karunakaran, Chithra ^b   Tanino, Karen K ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b CANADIAN LIGHT SOURCE INC   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

WATER; WAX;

ADAPTATION; ANATOMY AND HISTOLOGY; CHEMISTRY; CLASSIFICATION; DROUGHT; INFRARED SPECTROSCOPY; METABOLISM; PHYSIOLOGICAL STRESS; PLANT LEAF; SCANNING ELECTRON MICROSCOPY; SPECIES DIFFERENCE; SYNCHROTRON; ULTRASTRUCTURE; WHEAT; X RAY ABSORPTION SPECTROSCOPY;

ADAPTATION, PHYSIOLOGICAL; DROUGHTS; MICROSCOPY, ELECTRON, SCANNING; PLANT LEAVES; SPECIES SPECIFICITY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STRESS, PHYSIOLOGICAL; SYNCHROTRONS; TRITICUM; WATER; WAXES; X-RAY ABSORPTION SPECTROSCOPY;

EID: 85032890675     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12637     Document Type: Article

References (72)

1. Baenziger PS, Wesenberg DM, Sicher RC (1983) The effects of genes controlling barley leaf and sheath waxes on agronomic performance in irrigated and dryland environments. Crop Sci 23: 116–120
2. Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Bot J Linn Soc 126: 237–260
3. Bengston C, Larsson S, Liljenberg C (1978) Effect of water stress on cuticular transpiration rate and amount and composition of epicuticular wax in seedlings of six oat varieties. Physiol Plant 44: 319–324
4. Bi H, Luang S, Li Y, Bazanova N, Morran S, Song Z, Perera MA, Hrmova M, Borisjuk N, Lopato S (2016) Identification and characterization of wheat drought-responsive MYB transcription factors involved in the regulation of cuticle biosynthesis. J Exp Bot 67: 5363–5380
5. Bi H, Kovalchuk N, Langridge P, Tricker PJ, Lopato S, Borisjuk N (2017) The impact of drought on wheat leaf cuticle properties. BMC Plant Biol 17: 85
6. Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140: 176–183
7. Clarke JM (1986) Effect of leaf rolling on leaf water loss in Triticum spp. Can J Plant Sci 66: 885–891
8. Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, Storme V, Clement L, Gonzalez N, Inzé D (2015) Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol 167: 800–816
9. Denčić S, Kastori R, Kobiljski B, Duggan B (2000) Evaluation of grain yield and its components in wheat cultivars and landraces under near optimal and drought conditions. Euphytica 113: 43–52
10. DePauw R, Knox R, Clarke F, Clarke J, McCaig T (2009) Stettler hard red spring wheat. Can J Plant Sci 89: 945–951
11. Donald CM, Hamblin J (1976) Biological yield and harvest index of cereals as agronomic and plant breeding criteria. Adv Agron 28: 361–405
12. Entz MH, Fowler DB (1988) Critical stress periods affecting productivity of no-till winter wheat in Western Canada. Agron J 80: 987–992
13. Esau K (1956) An anatomists view of virus diseases. Am J Bot 43: 739–748
14. Eslami M, Dehghanzadeh H (2014) The effect of zinc on yield and yield components of sunflower (Helianthus annuus L.) under drought stress. Sci J Crop Sci 3: 61–65
15. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33: 317–345
16. Febrero A, Fernández S, Molina-Cano JL, Araus JL (1998) Yield, carbon isotope discrimination, canopy reflectance and cuticular conductance of barley isolines of differing glaucousness. J Exp Bot 49: 1575–1581
17. Fischer RA, Maurer R (1978) Drought resistance in spring wheat cultivars. 1. Grain-yield response. Aust J Agric Res 29: 897–912
18. Fischer R, Rees D, Sayre K, Z-M L, Condon A, Saavedra AL (1998) Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci 38: 1467–1475
19. González A, Ayerbe L (2010) Effect of terminal water stress on leaf epicuticular wax load, residual transpiration and grain yield in barley. Euphytica 172: 341–349
20. Hajiboland R, Amirazad H (2010) Drought tolerance in Zn-deficient red cabbage (Brassica oleracea L. var. capitata f. rubra) plants. Hort Sci 37: 88–98
21. Harb A, Pereira A (2011) Screening Arabidopsis genotypes for drought stress resistance. Methods Mol Biol 678: 191–198
22. Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation and plant growth. Plant Physiol 154: 1254–1271
23. Hebbern CA, Laursen KH, Ladegaard AH, Schmidt SB, Pedas P, Bruhn D, Schjoerring JK, Wulfsohn D, Husted S (2009) Latent manganese deficiency increases transpiration in barley (Hordeum vulgare). Physiol Plant 135: 307–316
24. Jarvis P (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc Lond B Biol Sci 273: 593–610
25. Jeffree C, Baker E, Holloway P (1976) Origins of the fine structure of plant epicuticular waxes. In: Dickinson CH, Preece TF (eds) Microbiology of Aerial Plant Surfaces. London, Academic Press, pp 119–158
26. Jenks MA, Ashworth EN (1999) Plant epicuticular waxes: function, production, and genetics. In: Janick J (ed) Horticultural Reviews, Vol. 23. John Wiley and Sons Inc, New York, pp 1–54
27. Jenner G, Longerich H, Jackson S, Fryer B (1990) ICP-MS—a powerful tool for high-precision trace-element analysis in earth sciences: evidence from analysis of selected USGS reference samples. Chem Geol 83: 133–148
28. Jiang YF, Lahlali R, Karunakaran C, Kumar S, Davis AR, Bueckert RA (2015) Seed set, pollen morphology and pollen surface composition response to heat stress in field pea. Plant Cell Environ 38: 2387–2397
29. Johnson DA, Richards RA, Turner NC (1983) Cuticular conductance, water use efficiency and drought tolerance of durum wheat isolines of differing glaucousness. Crop Sci 23: 318–325
30. Jordan WR, Monk RL, Miller FR, Rosenow DT, Clark LE, Shouse PJ (1983) Environmental physiology of sorghum. I. Environmental and genetic control of epicuticular wax load. Crop Sci 23: 552–558
31. Kalcsits LA (2016) Non-destructive measurement of calcium and potassium in apple and pear using handheld X-ray fluorescence. Front Plant Sci 7: 442
32. Karim MR, Zhang YQ, Zhao RR, Chen XP, Zhang FS, Zou CQ (2012) Alleviation of drought stress in winter wheat by late foliar application of zinc, boron, and manganese. J Plant Nutr Soil Sci 175: 142–151
33. Koch K, Neinhuis C, Ensikat HJ, Barthlott W (2004) Self assembly of epicuticular waxes on living plant surfaces imaged by atomic force microscopy (AFM). J Exp Bot 55: 711–718
34. Lahlali R, Jiang Y, Kumar S, Karunakaran C, Liu X, Borondics F, Hallin E, Bueckert R (2014) ATR–FTIR spectroscopy reveals involvement of lipids and proteins of intact pea pollen grains to heat stress tolerance. Front Plant Sci 5: 747
35. Lahlali R, Karunakaran C, Wang L, Willick I, Schmidt M, Liu X, Borondics F, Forseille L, Fobert PR, Tanino K, Peng G, Hallin E (2015) Synchrotron based phase contrast X-ray imaging combined with FTIR spectroscopy reveals structural and biomolecular differences in spikelets play a significant role in resistance to Fusarium in wheat. BMC Plant Biol 15: 24
36. Lahlali R, Kumar S, Wang L, Forseille L, Sylvain N, Korbas M, Muir D, Swerhone G, Lawrence JR, Fobert PR, Peng G, Karunakaran C (2016) Cell wall biomolecular composition plays a potential role in the host type II resistance to Fusarium head blight in wheat. Front Microbiol 7: 910
37. Lee SB, Suh MC (2015) Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species. Plant Cell Rep 34: 557–572
38. Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529: 84–87
39. Levitt J (1980) Responses of Plants to Environmental Stresses, Vol. II. Water, Radiation, Salt, and Other Stresses. Academic Press: New York, NY, USA
40. Liu N, Yu P (2010) Characterization of the microchemical structure of seed endosperm within a cellular dimension among six barley varieties with distinct degradation kinetics, using ultraspatially resolved synchrotron-based infrared microspectroscopy. J Agric Food Chem 58: 7801
41. Lombardi L, Sebastiani L, Vitagliano C (2003) Physiological, biochemical, and molecular effects of in vitro induced iron deficiency in peach rootstock Mr. S 2/5. J Plant Nutr 26: 2149–2163
42. McLaren TI, Guppy CN, Tighe MK, Forster N, Grave P, Lisle LM, Bennett JW (2012) Rapid, nondestructive total elemental analysis of vertisol soils using portable X-ray fluorescence. Soil Sci Soc Am J 76: 1436–1445
43. Medrano H, Escalona JM, Bota J, Gulías J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot 89: 895–905
44. Millaleo R, Reyes-Díaz M, Ivanov A, Mora M, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10: 470–481
45. Millan-Oropeza A, Rebois R, David M, Moussa F, Dazzi A, Bleton J, Virolle MJ, Deniset-Besseau A (2017) Attenuated total reflection Fourier transform infrared (ATR FT-IR) for rapid determination of microbial cell lipid content: correlation with gas chromatography-mass spectrometry (GC-MS). Appl Spectrosc 1: 3702817709459. https://doi.org/10.1177/0003702817709459
46. O'Toole JC, Cruz RT (1983) Genetic variation in epicuticular wax of rice. Crop Sci 23: 392–394
47. Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13: 236–246
48. Premachandra G, Saneoka H, Kanaya M, Ogata S (1991) Cell membrane stability and leaf surface wax content as affected by increasing water deficits in maize. J Exp Bot 42: 167–171
49. Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59: 683–707
50. Sanchez FJ, Manzanares M, de Andres EF, Tenorio JL, Ayerbe L (2001) Residual transpiration rate, epicuticular wax load and leaf colour of pea plants in drought conditions. Influence on harvest index and canopy temperature. Eur J Agron 15: 57–70
51. Schneider LM, Adamski NM, Christensen CE, Stuart DB, Vautrin S, Hansson M, Uauy C, von Wettstein-Knowles P (2016) The Cer-cqu gene cluster determines three key players in a β-diketone synthase polyketide pathway synthesizing aliphatics in epicuticular waxes. J Exp Bot 67: 2715–2730
52. Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicators. Crop Sci 28: 526–531
53. Shepherd T, Griffiths WD (2006) The effects of stress on plant cuticular waxes. New Phytol 171: 469–499
54. Shiferaw B, Smale M, Braun H-J, Duveiller E, Reynolds M, Muricho G (2013) Crops that feed the world. 10 past successes and future challenges to the role played by wheat in global food security. Food Secur 5: 291–317
55. Sowa S, Towill LE (1991) Infrared spectroscopy of plant cell cultures noninvasive measurement of viability. Plant Physiol 95: 610–615
56. Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16: 341–349
57. Townley-Smith TF, Humphreys DG, Czarnecki E, Lukow OM, McCallum BM, Fetch TG, Gilbert JA, Menzies JG, Brown PD (2010) Superb hard red spring wheat. Can J Plant Sci 90: 347–352
58. Tulloch AP (1973) Composition of leaf surface waxes of Triticum species: variation with age and tissue. Phytochemistry 12: 2225–2232
59. Uddin MN, Marshall DR (1988) Variation in epicuticular wax content in wheat. Euphytica 38: 3–9
60. Vijayan P, Willick IR, Lahlali R, Karunakaran C, Tanino KK (2015) Synchrotron radiation sheds fresh light on plant research: the use of powerful techniques to probe structure and composition of plants. Plant Cell Physiol 56: 1252–1263
61. von Wettstein-Knowles P (1972) Genetic control of β-diketone and hydroxy-β-diketone synthesis in epicuticular waxes of barley. Planta 106: 113–130
62. Walker AM, Yu P, Christensen CR, Christensen DA, McKinnon JJ (2009) Fourier transform infrared microspectroscopic analysis of the effects of cereal type and variety within a type of grain on structural makeup in relation to rumen degradation kinetics. J Agric Food Chem 57: 6871–6878
63. Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B (2014) Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J Exp Bot 65: 6441–6456
64. Wang Y, Jiahuan W, Guaiqiang C, Chunlian L, Yingang H, Xinhong C, Zhonghua W (2015a) Developmental changes in composition and morphology of cuticular waxes on leaves and spikes of glossy and glaucous wheat (Triticum aestivum L.) PLoS One 10: e0141239
65. Wang W, Liu X, Gai X, Ren J, Liu X, Cai Y, Wang Q, Ren H (2015b) Cucumis sativus L. WAX2 plays a pivotal role in wax biosynthesis, influencing pollen fertility and plant biotic and abiotic stress responses. Plant Cell Physiol 56: 1339–1354
66. Wang M, Wang Y, Wu H, Xu J, Li T, Hegebarth D, Jetter R, Chen L, Wang Z (2016) Three TaFAR genes function in the biosynthesis of primary alcohols and the response to abiotic stresses in Triticum aestivum. Sci Rep 6: 25008
67. Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kumar D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson LT, van Zyl L, Egertsdotter U, Sederoff RR, Grene R (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 133: 1702–1716
68. Weatherley PE (1950) Studies in the water relations of the cotton plant. I. The field measurement of water deficits in leaves. New Phytol 49: 81–97
69. Wu S, Hu C, Tan Q, Li L, Shi K, Zheng Y, Sun X (2015) Drought stress tolerance mediated by zinc-induced antioxidative defense and osmotic adjustment in cotton (Gossypium hirsutum). Acta Physiol Plant 37: 167
70. Xin H, Zhang X, Yu P (2013) Using synchrotron radiation-based infrared microspectroscopy to reveal microchemical structure characterization: frost damaged wheat vs. normal wheat. Int J Mol Sci 14: 16706–16718
71. Zadoks JC, Chang TT, Konzak CF (1974) Decimal code for growth stages of cereals. Weed Res 14: 415–421
72. Zhang ZZ, Wang W, Li WL (2013) Genetic interactions underlying the biosynthesis and inhibition of beta-diketones in wheat and their impact on glaucousness and cuticle permeability. PLoS One 8: e54129