Tree tobacco (Nicotiana glauca) cuticular wax composition is essential for leaf retention during drought, facilitating a speedy recovery following rewatering.
Nicotiana glauca
alkanes
drought
epicuticular wax
fatty alcohols
genome editing
plant fitness
tree tobacco
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
01
08
2022
accepted:
05
11
2022
pubmed:
13
11
2022
medline:
4
2
2023
entrez:
12
11
2022
Statut:
ppublish
Résumé
Despite decades of extensive study, the role of cuticular lipids in sustaining plant fitness is far from being understood. We utilized genome-edited tree tobacco (Nicotiana glauca) to investigate the significance of different classes of epicuticular wax in abiotic stress such as cuticular water loss, drought, and light response. We generated mutants displaying a range of wax compositions. Four wax mutants and one cutin mutant were extensively investigated for alterations in their response to abiotic factors. Although the mutations led to elevated cuticular water loss, the wax mutants did not display elevated transpiration or reduced growth under nonstressed conditions. However, under drought, plants lacking alkanes were unable to reduce their transpiration, leading to leaf death, impaired recovery, and stem cracking. By contrast, plants deficient in fatty alcohols exhibited elevated drought tolerance, which was part of a larger trend of plant phenotypes not clustering by a glossy/glaucous appearance in the parameters examined in this study. We conclude that although alkanes have little effect on whole N. glauca transpiration and biomass gain under normal, nonstressed conditions, they are essential during drought responses, since they enable plants to seal their cuticle upon stomatal closure, thereby reducing leaf death and facilitating a speedy recovery.
Substances chimiques
Water
059QF0KO0R
Alkanes
0
Waxes
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1574-1589Informations de copyright
© 2022 The Authors New Phytologist © 2022 New Phytologist Foundation.
Références
Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A. 1995. Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 11: 825-838.
Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Domínguez E, Wang Z, De Vos RCH, Jetter R et al. 2009. Fruit-surface flavonoid accumulation in tomato is controlled by a SLMYB12-regulated transcriptional network. PLoS Genetics 5: e1000777.
Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A. 2004. The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480.
Alcerito T, Barbo FE, Negri G, Santos DYAC, Meda CI, Young MCM, Chávez D, Blatt CTT. 2002. Foliar epicuticular wax of Arrabidaea brachypoda: flavonoids and antifungal activity. Biochemical Systematics and Ecology 30: 677-683.
Bach L, Michaelson LV, Haslam R, Bellec Y, Gissot L, Marion J, Da Costa M, Boutin J-P, Miquel M, Tellier F et al. 2008. The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proceedings of the National Academy of Sciences, USA 105: 14727-14731.
Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H. 1998. Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126: 237-260.
Beaudoin F, Wu X, Li F, Haslam RP, Markham JE, Zheng H, Napier JA, Kunst L. 2009. Functional characterization of the Arabidopsis β-ketoacyl-coenzyme a reductase candidates of the fatty acid elongase. Plant Physiology 150: 1174-1191.
Bickford CP. 2016. Ecophysiology of leaf trichomes. Functional Plant Biology 43: 807-814.
Bourdenx B, Bernard A, Domergue F, Pascal S, Leger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA et al. 2011. Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiology 156: 29-45.
Cameron AD. 2019. Mitigating the risk of drought-induced stem cracks in conifers in a changing climate. Scandinavian Journal of Forest Research 34: 667-672.
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 Physiology 140: 176-183.
Cameron RJ. 1970. Light intensity and the growth of Eucalyptus seedlings. The effect of cuticular waxes on light absorption in leaves of Eucalyptus species. Australian Journal of Botany 18: 275-284.
Chalker-Scott L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70: 1-9.
Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA. 2003. Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15: 1170-1185.
Cohen H, Dong Y, Szymanski J, Lashbrooke J, Meir S, Almekias-Siegl E, Zeisler-Diehl VV, Schreiber L, Aharoni A. 2019. A multilevel study of melon fruit reticulation provides insight into skin ligno-suberization hallmarks. Plant Physiology 179: 1486-1501.
Dalal A, Shenhar I, Bourstein R, Mayo A, Grunwald Y, Averbuch N, Attia Z, Wallach R, Moshelion M. 2020. A telemetric, gravimetric platform for real-time physiological phenotyping of plant-environment interactions. Journal of Visualized Experiments 2020: 1-28.
Eigenbrode SD, Espelie KE. 1995. Effects of plant epicuticular lipids on insect herbivores. Annual Review of Entomology 40: 171-194.
Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L, Jetter R. 2007. The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiology 145: 653-667.
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8: 1494-1512.
Halperin O, Gebremedhin A, Wallach R, Moshelion M. 2017. High-throughput physiological phenotyping and screening system for the characterization of plant-environment interactions. The Plant Journal 89: 839-850.
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM. 2007. Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics 8: 157-178.
Hen-Avivi S, Savin O, Racovita RC, Lee W-S, Adamski NM, Malitsky S, Almekias-Siegl E, Levy M, Vautrin S, Bergès H et al. 2016. A metabolic gene cluster in the wheat W1 and the barley Cer-cqu loci determines b-diketone biosynthesis and glaucousness. Plant Cell 28: 1440-1460.
Jetter R, Riederer M. 2016. Localization of the transpiration barrier in the epi- and intracuticular waxes of eight plant species: water transport resistances are associated with fatty acyl rather than alicyclic components. Plant Physiology 170: 921-934.
Lange H, Ndecky SYA, Gomez-Diaz C, Pflieger D, Butel N, Zumsteg J, Kuhn L, Piermaria C, Chicher J, Christie M et al. 2019. RST1 and RIPR connect the cytosolic RNA exosome to the Ski complex in Arabidopsis. Nature Communications 10: 3871.
Lee SB, Kim H, Kim RJ, Suh MC. 2014. Overexpression of Arabidopsis MYB96 confers drought resistance in Camelina sativa via cuticular wax accumulation. Plant Cell Reports 33: 1535-1546.
Lee SB, Suh MC. 2015. Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species. Plant Cell Reports 34: 557-572.
Leide J, Hildebrandt U, Reussing K, Riederer M, Vogg G. 2007. The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a β-ketoacyl-coenzyme A synthase (LeCER6). Plant Physiology 144: 1667-1679.
Leide J, Hildebrandt U, Vogg G, Riederer M. 2011. The positional sterile (ps) mutation affects cuticular transpiration and wax biosynthesis of tomato fruits. Journal of Plant Physiology 168: 871-877.
Li F, Wu X, Lam P, Bird D, Zheng H, Samuels L, Jetter R, Kunst L. 2008. Identification of the wax ester synthase/acyl-coenzyme A:diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiology 148: 97-107.
Liu N, Chen J, Wang T, Li Q, Cui P, Jia C, Hong Y. 2019. Overexpression of WAX INDUCER1/SHINE1 gene enhances wax accumulation under osmotic stress and oil synthesis in Brassica napus. International Journal of Molecular Sciences 20: 4435.
Long LM, Prinal Patel H, Cory WC, Stapleton AE. 2003. The maize epicuticular wax layer provides UV protection. Functional Plant Biology 30: 75-81.
Long N, Ren X, Xiang Z, Wan W, Dong Y. 2016. Sequencing and characterization of leaf transcriptomes of six diploid Nicotiana species. Journal of Biological Research 23: 6.
Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA. 2009. Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. The Plant Journal 59: 553-564.
Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, Kunst L, Michael Giblin E, Taylor DC, Kunst L. 1999. CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11: 825-838.
Millar AA, Kunst L. 1997. Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme. The Plant Journal 12: 121-131.
Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A et al. 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology 147: 823-851.
Mortimer CL, Bramley PM, Fraser PD. 2012. The identification and rapid extraction of hydrocarbons from Nicotiana glauca: a potential advanced renewable biofuel source. Phytochemistry Letters 5: 455-458.
Negin B, Moshelion M. 2017. The advantages of functional phenotyping in pre-field screening for drought-tolerant crops. Functional Plant Biology 44: 107-118.
Pascal S, Bernard A, Deslous P, Gronnier J, Fournier-Goss A, Domergue F, Rowland O, Joubès J. 2019. Arabidopsis CER1-LIKE1 functions in a cuticular very-long-chain alkane-forming complex. Plant Physiology 179: 415-432.
Peiffer M, Tooker JF, Luthe DS, Felton GW. 2009. Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytologist 184: 644-656.
Richards R, Rawson H, Johnson D. 1986. Glaucousness in wheat: its development and effect on water-use efficiency, gas exchange and photosynthetic tissue temperatures. Functional Plant Biology 13: 465.
Roth-Nebelsick A, Fernández V, Peguero-Pina JJ, Sancho-Knapik D, Gil-Pelegrín E. 2013. Stomatal encryption by epicuticular waxes as a plastic trait modifying gas exchange in a Mediterranean evergreen species (Quercus coccifera L.). Plant, Cell & Environment 36: 579-589.
Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L. 2006. CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiology 142: 866-877.
Ryan KG, Swinny EE, Markham KR, Winefield C. 2002. Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves. Phytochemistry 59: 23-32.
Ryan KG, Swinny EE, Winefield C, Markham KR. 2001. Flavonoids and UV photoprotection in Arabidopsis mutants. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 56: 745-754.
Sarrion-Perdigones A, Vazquez-Vilar M, Palací J, Castelijns B, Forment J, Ziarsolo P, Blanca J, Granell A, Orzaez D. 2013. Goldenbraid 2.0: a comprehensive DNA assembly framework for plant synthetic biology. Plant Physiology 162: 1618-1631.
Schnurr J, Shockey J, Browse J. 2004. The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16: 629-642.
Seo PJ, Lee SB, Suh MC, Park MJ, Park CM. 2011. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23: 1138-1152.
Simpson JP, Ohlrogge JB. 2016. A novel pathway for triacylglycerol biosynthesis is responsible for the accumulation of massive quantities of glycerolipids in the surface wax of bayberry (Myrica pensylvanica) fruit. Plant Cell 28: 248-264.
Sonawane PD, Jozwiak A, Panda S, Aharoni A. 2020. ‘Hijacking’ core metabolism: a new panache for the evolution of steroidal glycoalkaloids structural diversity. Current Opinion in Plant Biology 55: 118-128.
Steffens JC, Walters DS. 1991. Biochemical aspects of glandular trichome-mediated insect resistance in the Solanaceae. ACS Symposium Series 449: 136-149.
Usadel B, Tohge T, Scossa F, Sierro N, Schmidt M, Vogel A, Bolger A, Kozlo A, Enfissi EM, Morrel K et al. 2018. The genome and metabolome of the tobacco tree, Nicotiana glauca: a potential renewable feedstock for the bioeconomy. bioRxiv. doi: 10.1101/351429.
Xue D, Zhang X, Lu X, Chen G, Chen ZH. 2017. Molecular and evolutionary mechanisms of cuticular wax for plant drought tolerance. Frontiers in Plant Science 8: 621.
Yaaran A, Negin B, Moshelion M. 2019. Role of guard-cell ABA in determining maximal stomatal aperture and prompt vapor-pressure-deficit response. Plant Science 281: 31-40.
Yeats TH, Rose JKC. 2013. The formation and function of plant cuticles. Plant Physiology 163: 5-20.
Zeisler V, Schreiber L. 2016. Epicuticular wax on cherry laurel (Prunus laurocerasus) leaves does not constitute the cuticular transpiration barrier. Planta 243: 65-81.
Zeisler-Diehl V, Müller Y, Schreiber L. 2018. Epicuticular wax on leaf cuticles does not establish the transpiration barrier, which is essentially formed by intracuticular wax. Journal of Plant Physiology 227: 66-74.
Zeltińš P, Katrevičs J, Gailis A, Maaten T, Baders E, Jansons A. 2018. Effect of stem diameter, genetics, and wood properties on stem cracking in Norway spruce. Forests 9: 546.
Zheng H, Rowland O, Kunst L. 2005. Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17: 1467-1481.