Isoprene emission protects photosynthesis but reduces plant productivity during drought in transgenic tobacco (Nicotiana tabacum) plants

New Phytologist

Volumn 201, Issue 1, 2014, Pages 205-216

  Ryan, Annette C ^a   Hewitt, C Nicholas ^a   Possell, Malcolm ^b   Vickers, Claudia E ^c   Purnell, Anna ^a   Mullineaux, Philip M ^d   Davies, William J ^a   Dodd, Ian C ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

Abscisic acid (ABA); Drought; Hydrogen peroxide; Isoprene; Lipid peroxidation; Nicotiana tabacum (tobacco); Oxidative stress; Water use efficiency

Indexed keywords

ABSCISIC ACID; BIOGENIC EMISSION; BIOLOGICAL PRODUCTION; DROUGHT; FUNCTIONAL ROLE; HYDROGEN PEROXIDE; ISOPRENE; LIPID; PHOTOCHEMISTRY; PHOTOSYNTHESIS; TOBACCO; TRANSGENIC PLANT; WATER USE EFFICIENCY; WILTING;

NICOTIANA TABACUM;

1,3 BUTADIENE DERIVATIVE; ABSCISIC ACID; HEMITERPENE; HYDROGEN PEROXIDE; ISOPRENE; PENTANE; PHYTOHORMONE; REACTIVE OXYGEN METABOLITE; WATER;

ABSCISIC ACID (ABA); ARTICLE; BIOMASS; DROUGHT; GROWTH, DEVELOPMENT AND AGING; LIPID PEROXIDATION; METABOLISM; NICOTIANA TABACUM (TOBACCO); OXIDATIVE STRESS; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; PLANT LEAF; PLANT WATER USE; TOBACCO; TRANSGENIC PLANT;

ABSCISIC ACID (ABA); DROUGHT; HYDROGEN PEROXIDE; ISOPRENE; LIPID PEROXIDATION; NICOTIANA TABACUM (TOBACCO); OXIDATIVE STRESS; WATER USE EFFICIENCY;

ABSCISIC ACID; BIOMASS; BUTADIENES; DROUGHTS; HEMITERPENES; LIPID PEROXIDATION; OXIDATIVE STRESS; PENTANES; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; TOBACCO; WATER;

EID: 84888289430     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12477     Document Type: Article

References (68)

1. Asada K. 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141: 391-396.
2. Barta C, Loreto F. 2006. The relationship between the methyl-erythritol phosphate pathway leading to emission of volatile isoprenoids and abscisic acid content in leaves. Plant Physiology 141: 1676-1683.
3. Beckett M, Loreto F, Velikova V, Brunetti C, Di Ferdinando M, Tattini M, Calfapietra C, Farrant JM. 2012. Photosynthetic limitations and volatile and non-volatile isoprenoids in the poikilochlorophyllous resurrection plant Xerophyta humilis during dehydration and rehydration. Plant, Cell & Environment 35: 2061-2074.
4. Begcy K, Mariano ED, Mattiello L, Nunes AV, Mazzafera P, Maia IG, Menossi M. 2011. An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants. PLoS ONE 6: e23776.
5. Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hasch R, Polle A, Bohlmann J, Schnitzler JP. 2007. Transgenic, non-isoprene emitting poplars don′t like it hot. Plant Journal 51: 485-499.
6. Behnke K, Grote R, Bruggemann N, Zimmer I, Zhou GW, Elobeid M, Janz D, Polle A, Schnitzler JP. 2012. Isoprene emission-free poplars - a chance to reduce the impact from poplar plantations on the atmosphere. New Phytologist 194: 70-82.
7. Blum A. 2005. Drought resistance, water-use efficiency, and yield potential - are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research 56: 1159-1168.
8. Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M. 2007. Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytologist 175: 244-254.
9. Bruggemann N, Schnitzler JP. 2002. Comparison of isoprene emission, intercellular isoprene concentration and photosynthetic performance in water-limited oak (Quercus pubescens Willd and Quercus robur L.) saplings. Plant Biology 4: 456-463.
10. Centritto M, Brilli F, Fodale R, Loreto F. 2011. Different sensitivity of isoprene emission, respiration and photosynthesis to high growth temperature coupled with drought stress in black poplar (Populus nigra) saplings. Tree Physiology 31: 275-286.
11. Chaves MM, Maroco JP, Pereira JS. 2003. Understanding plant responses to drought - from genes to the whole plant. Functional Plant Biology 30: 239-264.
12. Dai A. 2011. Drought under global warming: a review. Wiley Interdisciplinary Reviews: Climate Change 2: 45-65.
13. DemmigAdams B, Adams WW, Barker DH, Logan BA, Bowling DR, Verhoeven AS. 1996. Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98: 253-264.
14. Dodd IC, Egea G, Watts CW, Whalley WR. 2010. Root water potential integrates discrete soil physical properties to influence ABA signalling during partial rootzone drying. Journal of Experimental Botany 61: 3543-3551.
15. Fang CW, Monson RK, Cowling EB. 1996. Isoprene emission, photosynthesis, and growth in sweetgum (Liquidambar styraciflua) seedlings exposed to short- and long-term drying cycles. Tree Physiology 16: 441-446.
16. 2 concentration. New Phytologist 172: 73-82.
17. Fortunati A, Barta C, Brilli F, Centritto M, Zimmer I, Schnitzler J-P, Loreto F. 2008. Isoprene emission is not temperature-dependent during and after severe drought-stress: a physiological and biochemical analysis. The Plant Journal 55: 687-697.
18. Griffiths H, Parry MAJ. 2002. Plant responses to water stress - preface. Annals of Botany 89: 801-802.
19. Hartung W, Sauter A, Hose E. 2002. Abscisic acid in the xylem: where does it come from, where does it go to? Journal of Experimental Botany 53: 27-32.
20. Heath RL, Packer L. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry & Biophysics 125: 189-198.
21. Hussain MZ, Vanloocke A, Siebers MH, Ruiz-Vera UM, Markelz RJC, Leakey ADB, Ort DR, Bernacchi CJ. 2013. Future carbon dioxide concentration decreases canopy evapotranspiration and soil water depletion by field-grown maize. Global Change Biology 19: 1572-1584.
22. Jones HG. 1987. Correction for nonspecific interference in competitive immunoassys. Physiologia Plantarum 70: 146-154.
23. Krieger-Liszkay A. 2005. Singlet oxygen production in photosynthesis. Journal of Experimental Botany 56: 337-346.
24. Lawlor DW, Tezara W. 2009. Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Annals of Botany 103: 561-579.
25. Loivamaeki M, Gilmer F, Fischbach RJ, Soergel C, Bachl A, Walter A, Schnitzler J-P. 2007. Arabidopsis, a model to study biological functions of isoprene emission? Plant Physiology 144: 1066-1078.
26. Loreto F, Mannozzi M, Maris C, Nascetti P, Ferranti F, Pasqualini S. 2001. Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiology 126: 993-1000.
27. Magel E, Mayrhofer S, Muller A, Zimmer I, Hampp R, Schnitzler JP. 2006. Photosynthesis and substrate supply for isoprene biosynthesis in poplar leaves. Atmospheric Environment 40: 138-151.
28. Martin-Vertedor AI, Dodd IC. 2011. Root-to-shoot signalling when soil moisture is heterogeneous: increasing the proportion of root biomass in drying soil inhibits leaf growth and increases leaf abscisic acid concentration. Plant, Cell & Environment 34: 1164-1175.
29. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33: 453-467.
30. Mishra G, Zhang WH, Deng F, Zhao J, Wang XM. 2006. A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312: 264-266.
31. Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, K-i Tomizawa. 2005. Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant and Cell Physiology 46: 1819-1830.
32. Molinier J, Ries G, Zipfel C, Hohn B. 2006. Transgeneration memory of stress in plants. Nature 442: 1046-1049.
33. Monson RK, Trahan N, Rosenstiel TN, Veres P, Moore D, Wilkinson M, Norby RJ, Volder A, Tjoelker MG, Briske DD et al. 2007. Isoprene emission from terrestrial ecosystems in response to global change: minding the gap between models and observations. Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences 365: 1677-1695.
34. 3 plants: a predominant role for photorespiration? Annals of Botany 89: 841-850.
35. Ozfidan C, Turkan I, Sekmen AH, Seckin B. 2011. Abscisic acid-regulated responses of aba2-1 under osmotic stress: the abscisic acid-inducible antioxidant defence system and reactive oxygen species production. Plant Biology 14: 337-346.
36. Parry MAJ, Andralojc PJ, Khan S, Lea PJ, Keys AJ. 2002. Rubisco activity: effects of drought stress. Annals of Botany 89: 833-839.
37. Pegoraro E, Rey ANA, Abrell L, Haren J, Lin G. 2006. Drought effect on isoprene production and consumption in Biosphere 2 tropical rainforest. Global Change Biology 12: 456-469.
38. Pegoraro E, Rey A, Greenberg J, Harley P, Grace J, Malhi Y, Guenther A. 2004. Effect of drought on isoprene emission rates from leaves of Quercus virginiana. Mill. Atmospheric Environment 38: 6149-6156.
39. Penuelas J, Munne-Bosch S. 2005. Isoprenoids: an evolutionary pool for photoprotection. Trends in Plant Science 10: 166-169.
40. Quarrie SA, Whitford PN, Appleford NEJ, Wang TL, Cook SK, Henson IE, Loveys BR. 1988. A monoclonal-antibody to (S)-Abscisic acid - its characterization and use in a radioimmunoassay for measuring abscisic-acid in crude extracts of cereal and lupin leaves. Planta 173: 330-339.
41. Rasulov B, Copolovici L, Laisk A, Niinemets U. 2009. Postillumination isoprene emission: in vivo measurements of dimethylallyldiphosphate pool size and isoprene synthase kinetics in aspen leaves. Plant Physiology 149: 1609-1618.
42. Rasulov B, Hueve K, Bichele I, Laisk A, Niinemets U. 2010. Temperature response of isoprene emission in vivo reflects a combined effect of substrate limitations and isoprene synthase activity: a kinetic analysis. Plant Physiology 154: 1558-1570.
43. Reddy AR, Chaitanya KV, Vivekanandan M. 2004. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology 161: 1189-1202.
44. Riga P, Vartanian N. 1999. Sequential expression of adaptive mechanisms is responsible for drought resistance in tobacco. Australian Journal of Plant Physiology 26: 211-220.
45. Rodeghiero M, Niinemets ULO, Cescatti A. 2007. Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar et al. model parameters? Plant, Cell and Environment 30: 1006-1022.
46. Ryan A, Cojocariu C, Possell M, Davies WJ, Hewitt CN. 2009. Defining hybrid poplar (Populus deltoides x Populus trichocarpa) tolerance to ozone: identifying key parameters. Plant, Cell & Environment 32: 31-45.
47. Sasaki K, Saito T, Lamsa M, Oksman-Caldentey KM, Suzuki M, Ohyama K, Muranaka T, Ohara K, Yazaki K. 2007. Plants utilize isoprene emission as a thermotolerance mechanism. Plant and Cell Physiology 48: 1254-1262.
48. Schachtman DP, Goodger JQD. 2008. Chemical root to shoot signaling under drought. Trends in Plant Science 13: 281-287.
49. Sharkey TD. 2013. Is it useful to ask why plants emit isoprene? Plant, Cell & Environment 36: 517-520.
50. Sharkey TD, Chen X, Yeh S. 2001. Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiology 125: 2001-2006.
51. Sharkey TD, Singsaas EL. 1995. Why plants emit isoprene. Nature 374: 769.
52. Sharkey TD, Wiberley AE, Donohue AR. 2007. Isoprene emission from plants: why and how. Annals of Botany 101: 5-18.
53. Sharkey TD, Yeh SS. 2001. Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology 52: 407-436.
54. Singsaas EL, Lerdau M, Winter K, Sharkey TD. 1997. Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiology 115: 1413-1420.
55. Stokes NJ, Lucas PW, Hewitt CN. 1993. Controlled environment fumigation chambers for the study of reactive air pollutant effects on plants. Atmospheric Environment Part A-General Topics 27: 679-683.
56. Suzuki N, Koussevitzky S, Mittler RON, Miller GAD. 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment 35: 259-270.
57. Taipale R, Ruuskanen TM, Rinne J, Kajos MK, Hakola H, Pohja T, Kulmala M. 2008. Technical Note: quantitative long-term measurements of VOC concentrations by PTR-MS - measurement, calibration, and volume mixing ratio calculation methods. Atmospheric Chemistry and Physics 8: 6681-6698.
58. Velikova V, Edreva A, Loreto F. 2004. Endogenous isoprene protects Phragmites australis leaves against singlet oxygen. Physiologia Plantarum 122: 219-225.
59. Velikova V, Pinelli P, Loreto F. 2005. Consequences of inhibition of isoprene synthesis in Phragmites australis leaves exposed to elevated temperatures. Agriculture, Ecosystems & Environment 106: 209-217.
60. Velikova V, Sharkey TD, Loreto F. 2012. Stabilization of thylakoid membranes in isoprene-emitting plants reduces formation of reactive oxygen species. Plant Signaling & Behavior 7: 139-141.
61. Velikova V, Varkonyi Z, Szabo M, Maslenkova L, Nogues I, Kovacs L, Peeva V, Busheva M, Garab G, Sharkey TD et al. 2011. Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiology 157: 905-916.
62. Vickers CE, Gershenzon J, Lerdau MT, Loreto F. 2009a. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nature Chemical Biology 5: 283-291.
63. Vickers CE, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Mullineaux PM, Hewitt CN. 2009b. Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant, Cell & Environment 32: 520-531.
64. Vickers CE, Possell M, Hewitt CN, Mullineaux PM. 2010. Genetic structure and regulation of isoprene synthase in Poplar (Populus spp.). Plant Molecular Biology 73: 547-558.
65. Vickers CE, Possell M, Laothawornkitkul J, Ryan AC, Hewitt CN, Mullineaux PM. 2011. Isoprene synthesis in plants: lessons from a transgenic tobacco model. Plant, Cell & Environment 34: 1043-1053.
66. Wiberley AE, Donohue AR, Westphal MM, Sharkey TD. 2009. Regulation of isoprene emission from poplar leaves throughout a day. Plant, Cell & Environment 32: 939-947.
67. Wolfertz M, Sharkey TD, Boland W, Kuhnemann F. 2004. Rapid regulation of the methylerythritol 4-phosphate pathway during isoprene synthesis. Plant Physiology 135: 1939-1945.
68. Zhou Y, Lam HM, Zhang J. 2007. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. Journal of Experimental Botany 58: 1207-1217.