Abstract
Jasmonates (JAs), a type of phytohormone, are involved in sensing and signaling of several environmental stresses (biotic and abiotic). Jasmonic acid (JA) has been suggested to function in plant responses to drought, because this type of stress induces expression of several genes that also respond to JA. We investigated the involvement of JA and its precursor (12-oxo-phytodienoic acid; OPDA) on seedling morphological and physiological characteristics of two sunflower (Helianthus annuus) inbred lines with contrasting responses (sensitive vs. tolerant) to water stress. Our experimental treatments were based on moderate water stress (simulated by application of mannitol 400 mM) and on blocking of JA biosynthesis (by the chemical inhibitor salicylhydroxamic acid; SHAM). Water stress resulted in reduction of primary root (PR) growth and lateral root (LR) growth, but in increased LR number. SHAM treatment increased PR length, LR number, and LR length, thus strongly affecting root architecture. Water stress had differential effects on various physiological parameters, including relative water content (RWC), stomatal conductance, and content of photosynthetic pigments (chlorophylls, carotenoids). OPDA and JA accumulation in aerial part and roots induced by water stress was reversed by combined water stress plus SHAM treatment at day 14. Our findings suggest that SHAM effectively inhibits de novo JA biosynthesis induced by water stress, and that JAs play a protective role in responses of sunflower seedlings to this stress. JAs, particularly OPDA, are highly effective signaling molecules in mediation of sunflower seedling responses to water stress.
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Abbreviations
- DAS:
-
Days after sowing
- JA:
-
Jasmonic acid
- JAs:
-
Jasmonates
- JA-Ile:
-
JA-isoleucine
- LR:
-
Lateral roots
- MPa:
-
Megapascal
- OPDA:
-
12-oxo-phytodienoic acid
- PR:
-
Primary root
- RWC:
-
Relative water content
- S + SHAM:
-
Water stress plus SHAM
- SHAM:
-
Salicylhydroxamic acid
- SD:
-
Stomatal density
- SI:
-
Stomatal index
References
Abdala G, Miersch O, Kramell R, Vigliocco A, Agostini E, Forchetti G, Alemano S (2003) Jasmonate and octadecanoid occurrence in tomato hairy roots. Endogenous level changes in response to NaCl. J Plant Growth Regul 40:21–27
Agele SO, Maraiyesa IO, Adeniji IA (2007) Effects of variety and row spacing on radiation interception, partitioning of dry matter and seed set efficiency in late season sunflower (Helianthus annuus L.) in a humid zone of Nigeria. Afr J Agric Res 2:080–088
Andrade A, Vigliocco A, Alemano S, Llanes A, Abdala G (2013) Comparative morpho-biochemical responses of sunflower lines sensitive and tolerant to water stress. Am J Plant Sci 4:156–167
Brossa R, López-Carbonell M, Jubany-Marí T, Alegre L (2011) Interplay between abscisic acid and jasmonic acid and its role in water-oxidative stress in wild-type, ABA-deficient, JA-deficient, and ascorbate-deficient plants. J Plant Growth Regul 30:322–333
Corti-Monzón G, Pinedo M, Lamattina L, de la Canal L (2012) Sunflower root growth regulation: the role of jasmonic acid and its relation with auxins. Plant Growth Regul 66:129–136
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679
Daszkowska-Golec A, Szarejko I (2013) Open or close the gate—stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138
De Domenico S, Bonsegna S, Horres R, Pastor V, Taurino M, Poltronieri P, Imtiaz M, Kahl G, Flors V, Winter P, Santino A (2012) Transcriptomic analysis of oxylipin biosynthesis genes and chemical profiling reveal an early induction of jasmonates in chickpea roots under drought stress. Plant Physiol Biochem 61:115–122
de Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306
Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:389–397
Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plants extracts by liquid chromatography-electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442
Farman A, Asghari B, Fazal A (2017) Recent methods of drought stress tolerance in plants. Plant Growth Regul 82:363–375
Feng H, Li H, Li X, Duan J, Liang H, Zhi D, Ma J (2007) The flexible interrelation between AOX respiratory pathway and photosynthesis in rice leaves. Plant Physiol Biochem 45:228–235
Gao XQ, Yang Q, Minami C, Matsuura H, Kimura A, Yoshihara T (2003) Inhibitory effect of salicylhydroxamic acid on theobroxide-induced potato tuber formation. Plant Sci 165:993–999
Gomes Gonçalves C, da Silva Junior AC, Rocha Pereira MR, Gasparino EC, Martins D (2017) Morphological modifications in soybean in response to soil water management. Plant Growth Regul 83:105–117
Grebner W, Stingl NE, Oenel A, Mueller MJ, Berger S (2013) Lipoxygenase6-dependent oxylipin synthesis in roots is required for abiotic and biotic stress resistance of Arabidopsis. Plant Physiol 161:2159–2170
Hamanishi ET, Thomas BR, Campbell MM (2012) Drought induces alterations in the stomatal development program in Populus. J Exp Bot 63:695–709
Kalve S, De Vos D, Beemster GTS (2014) Leaf development: a cellular perspective. Front Plant Sci 5:362
Kong F, Gao X, Nam KH, Takahashi K, Matsuura H, Yoshihara T (2005) Theobroxide inhibits stem elongation in Pharbitis nil by regulating jasmonic acid and gibberellin biosynthesis. Plant Sci 169:721–725
Lechner L, Pereyra-Irujo GA, Granier C, Aguirrezábal L (2008) Rewatering plants after a long water-deficit treatment reveals that leaf epidermal cells retain their ability to expand after the leaf has apparently reached its final size. Ann Bot 101:1007–1015
MacKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322
Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regul 53:43–50
Maksymiec W, Krupa Z (2007) Effects of methyl jasmonate and excess copper on root and leaf growth. Biol Plant 51:322–326
Manugistics (1997) Statgraphics plus for Windows 3.0. Manugistics, Rockville, MD
Meléndez-Martínez AJ, Vicario IM, Heredia FJ (2007) Review: analysis of carotenoids in orange juice. J Food Comp Anal 20:638–649
Meng L, Li L, Chen W, Xu Z, Liu L (1999) Effect of water stress on stomatal density, length, width and net photosynthetic rate in rice leaves. J Shenyang Agric Univ 30:477–480
Mo Y, Yang R, Liu L, Gu X, Yang X, Wang Y, Zhang X, Li H (2016) Growth, photosynthesis and adaptive responses of wild and domesticated watermelon genotypes to drought stress and subsequent re-watering. Plant Growth Regul 79:229–241
Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y (2007) The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol 143:1398–1407
Pedranzani H, Sierra-de-Grado R, Vigliocco A, Miersch O, Abdala G (2007) Cold and water stresses produce changes in endogenous jasmonates in two populations of Pinus pinaster Ait. Plant Growth Regul 52:111–116
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295
Poór P, Tari I (2012) Regulation of stomatal movement and photosynthetic activity in guard cells of tomato abaxial epidermal peels by salicylic acid. Funct Plant Biol 39:1028–1037
Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156
Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52(9):1569–1582
Rahbarian R, Khavari-Nejad R, Ganjeali A, Bagheri A, Najafi F (2011) Drought stress effects on photosynthesis, chlorophyll fluorescence and water relations in tolerant and susceptible chickpea (Cicer arietinum L.) genotypes. Acta Biol Cracov Ser Bot 53:47–56
Rudús I, Weiler EW, Kepczyńska E (2009) Do stress-related phytohormones, abscisic acid and jasmonic acid play a role in the regulation of Medicago sativa L. somatic embryogenesis? Plant Growth Regul 59:159–169
Savchenko T, Dehesh K (2014) Drought stress modulates oxylipin signature by eliciting 12-OPDA as a potent regulator of stomatal aperture. Plant Signal Behav 9:e28304
Savchenko T, Kolla VA, Wang CQ, Nasafi Z, Hicks DR, Phadungchob B, Chehab WE, Brandizzi F, Froehlich J, Dehesh K (2014) Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. Plant Physiol 164:1151–1160
Schneiter AA (1978) Non-destructive leaf area estimation in sunflower. Agron J 70:141–142
Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139
Turhan H, Baser I (2004) In vitro and in vivo water stress in sunflower (Helianthus annuus L.). Helia 27:227–236
Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366
Ünyayar S, Keles Y, Ünal E (2004) Proline and ABA levels in two sunflower genotypes subjected to water stress. Bulg J Physiol 30:34–47
van der Weele CM, Spollen WG, Sharp RE, Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J Exp Bot 51:1555–1562
Vernon LP (1960) Spectrophotometric determination of chlorophylls phaeophytins in plant extracts. Ann Chem 32:1144–1150
Waraich E, Ahmad R, Ashraf M, Saifullah Y, Ahmad M (2011) Improving agricultural water use efficiency by nutrient management in crop plants. Acta Agric Scand Sect B 61:291–304
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058
Wasternack C, Strnad M (2016) Jasmonate signaling in plant stress responses and development -active and inactive compounds. New Biot 33:604–613
Xin ZY, Zhou X, Pilet PE (1997) Level changes of jasmonic, abscisic, and indole-3yl-acetic acids in maize under desiccation stress. J Plant Physiol 151:120–124
Yordanov I, Velikova V, Tsonev T (2003) Plant responses to drought and stress tolerance. Bulg J Plant Physiol Special Issue 2003:187–206
Zhu C, Gan L, Shen Z, Xia K (2006) Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis. J Exp Bot 57:1299–1308
Image-Pro Plus - application notes. Silver Spring: Media Cybernetics (2002). http://www.mediacy.com/action.htm
Acknowledgements
This study was supported by grants from CONICET to AA, and from SECYT-UNRC to SA. The authors are grateful to Dr. S. Anderson for English editing of the manuscript.
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10725_2017_317_MOESM1_ESM.tif
Supplementary material 1 B59 seedlings grown under normal conditions (control) (A) and under water stress (mannitol 400 mM) (B) for 16 d. (TIF 2415 KB)
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Supplementary material 3 Leaf areas of B59 and B71 seedling under four experimental treatments as in Fig. 1. Data and statistical conventions as in Fig. 1. (TIFF 1915 KB)
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Supplementary material 4 Leaf growth rate of B59 seedlings grown under optimal conditions (control), water stress (mannitol 400 mM), SHAM treatment, and combination of water stress plus SHAM treatment (S + SHAM). Data shown are mean ± SE from four replicates. Values with the same letter are not significantly different at P ≤ 0.05. (TIFF 35 KB)
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Supplementary material 5 Leaf growth rate of B71 seedlings grown under four experimental treatments as in Fig. A3. Data and statistical conventions as in Fig. A3. (TIFF 2373 KB)
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Supplementary material 6 Microphotographs of abaxial and adaxial epidermis of B71 and B59 seedlings. Scale bar: 1 μm. (TIFF 7742 KB)
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Supplementary material 7 Stomatal density in leaves of B59 and B71 seedlings grown under four experimental treatments as in Fig. A3. Data and statistical conventions as in Fig. A3. (TIFF 127 KB)
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Supplementary material 8 Stomatal index in leaves of B59 and B71 seedlings grown under four experimental treatments as in Fig. A3. Data and statistical conventions as in Fig. A3, except with three replicates. (TIFF 126 KB)
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Andrade, A., Escalante, M., Vigliocco, A. et al. Involvement of jasmonates in responses of sunflower (Helianthus annuus) seedlings to moderate water stress. Plant Growth Regul 83, 501–511 (2017). https://doi.org/10.1007/s10725-017-0317-9
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DOI: https://doi.org/10.1007/s10725-017-0317-9