Water Stress-Induced Responses in the Growth, Cuticular Wax Composition, Chloroplast Pigments and Soluble Protein Content, and Redox Metabolism of Two Genotypes of Ricinus communis L.

Abstract

The aim of this study was to investigate the physiological and biochemical responses to three different water regimes in two castor bean genotypes (BRS Energia and BRS Nordestina) with different drought tolerance. After 67 days of sowing and 28 days under different water stress levels, some growth parameters were affected by increased stress, resulting in lower height, root, and shoot biomass, leaf area, and number of mature leaves. The increase in cuticular wax load on leaves was prominent under higher water stress. Triterpene and primary alcohols were the main constituent classes identified, but their content did not change under water deficit. Changes primarily occurred in the n-alkane and fatty acid classes. Water stress caused an increase in hydrogen peroxide and malondialdehyde content, a decrease in soluble protein content, and an increase in the activity of key enzymes of the antioxidant defense system (SOD, CAT, and APX). The BRS Nordestina genotype demonstrated a more efficient protection mechanism against drought compared to BRS Energia.

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References

  1. Ali F, Bano A, Fazal A (2017) Recent methods of drought stress tolerance in plants. Plant Growth Regul 82:363–375

    CAS  Google Scholar 

  2. Andrade FP, Freire EC, Lima EF, Silva GA, Silva LC, Dourado RMF (2010) BRS Nordestina. Embrapa Algodão, Campina Grande

    Google Scholar 

  3. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Env 24:1337–1344

    CAS  Google Scholar 

  4. Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in leaves and roots of wild-type and catalase-deficient mutant of barley. Physiol Plant 104:280–292

    CAS  Google Scholar 

  5. Baloğlu MC, Kavas M, Aydin G, Öktem HA, Yügel AM (2012) Antioxidative and physiological responses of two sunflower (Helianthus annuus) cultivars under PEG-mediated drought stress. Turk J Bot 36:707–714

    Google Scholar 

  6. Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plant 19:47–64

    CAS  Google Scholar 

  7. Bayat H, Moghadam, AN (2019) Drought effects on growth, water status, proline content and antioxidant system in three Salvia nemorosa L. cultivars. Acta Physiol. Plant 41:149.

  8. Bengtson C, Larsson S, Liljenberg C (1978) Effects 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

    CAS  Google Scholar 

  9. Berrs LSJ, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    Google Scholar 

  10. 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 17:1–13

    Google Scholar 

  11. Bondada BR, Oosterhuis DM, Murphy JB, Kim KS (1996) Effect of water stress on the epicuticular wax composition and ultrastructure of cotton (Gossypium hirsutum L.) leaves, bracts, and boll. Environ Exp Bot 36:61–69

    CAS  Google Scholar 

  12. Bourdenx B, Bernard A, Domergue F, Pascal S, Léger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Joubès J (2011) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol 156:29–45

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Buschhaus C, Jetter R (2012) Composition and physiological function of the wax layers coating Arabidopsis leaves: β-Amyrin negatively affects the intracuticular water barrier. Plant Physiol 160:1120–1129

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Cairo PAR (1995) Curso básico de relações hídricas de plantas. UESB, Vitória da Conquista

    Google Scholar 

  16. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Cassol D, Cruz FP, Espindola K, Mangeon A, Müller C, Loureiro ME, Corrêa RL, Sachetto-Martins G (2016) Identification of reference genes for quantitative RT-PCR analysis of microRNAs and mRNAs in castor bean (Ricinus communis L.) under drought stress. Plant Physiol Biochem 106:101–107

    CAS  PubMed  Google Scholar 

  18. Chakraborty U, Pradhan B (2012) Oxidative stress in five wheat varieties (Triticum aestivum L.) exposed to water stress and study of their antioxidant enzyme defense system, water stress responsive metabolites and H2O2 accumulation. Braz J Plant Physiol 24:117–130

    CAS  Google Scholar 

  19. Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    CAS  PubMed  Google Scholar 

  20. Claeys H, Inzé D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol 162:1768–1779

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Demidchik V (2015) Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environ Exp Bot 109:212–228

    CAS  Google Scholar 

  22. Duursma RA, Blackman CJ, Lopéz R, Martin-StPaul NK, Cochard H, Medlyn BE (2019) On the minimum leaf conductance: Its role in models of plant water use, and ecological and environmental controls. New Phytol 221:693–705

    PubMed  Google Scholar 

  23. Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: Plant responses and management options. Front Plant Sci 8:1–16

    Google Scholar 

  24. Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62:2599–2613

    CAS  PubMed  Google Scholar 

  25. Faria AP, Lemor-Filho JP, Modolo LV, França MGC (2013) Electrolyte leakage and chlorophyll a fluorescence among castor bean cultivars under induced water deficit. Acta Physiol Plant 35:119–128

    CAS  Google Scholar 

  26. Farmer EE, Mueller JM (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450

    CAS  PubMed  Google Scholar 

  27. Fathi A, Tari DB (2016) Effect of drought stress and its mechanism in plants. Int J Life Sci 10:1–16

    Google Scholar 

  28. Figueiredo KV, Oliveira MT, Oliveira AFM, Silva GC, Santos MG (2012) Epicuticular-wax removal influences gas exchange and water relations in the leaves of an exotic and native species from a Brazilian semiarid region under induced drought stress. Aust J Bot 60:685–692

    CAS  Google Scholar 

  29. Figueiredo KV, Oliveira MT, Arruda ECP, Silva BCF, Santos MG (2015) Changes in leaf epicuticular wax, gas exchange and biochemistry metabolism between Jatropha mollissima and Jatropha curcas under semi-arid conditions. Acta Physiol Plant 37:1–11

    CAS  Google Scholar 

  30. Franchini MC, Hernández LF, Lindstrom LI (2010) Cuticle and cuticular wax development in the sunflower (Helianthus annuus L.) pericarp grown at the field under a moderate water deficit. Phyton 79:153–161

    Google Scholar 

  31. Frosi G, Oliveira MT, Almeida-Cortez J, Santos MG (2013) Ecophysiological performance of Calotropis procera: an exotic and evergreen species in Caatinga, Brazilian semi-arid. Acta Physiol Plant 35:335–344

    Google Scholar 

  32. Gao S, Wang Y, Yu S, Huang Y, Liu H, Chen W, He X (2020) Effects of drought stress on growth, physiology and secondary metabolites of two Adonis species in Northeast China. Sci Hortic 259:108795

    CAS  Google Scholar 

  33. Giannopolitis CN, Ries SK (1977) Superoxide Dismutases: I. Occurrence in Higher Plants Plant Physiol 59:309–314

    CAS  PubMed  Google Scholar 

  34. Guhling O, Hobl B, Yeats T, Jetter R (2006) Cloning and characterization of a lupeol synthase involved in the synthesis of epicuticular wax crystals on stem and hypocotyl surfaces of Ricinus communis. Arch Biochem Biophys 448:60–72

    CAS  PubMed  Google Scholar 

  35. Guo J, Xu W, Yu X, Shen H, Li H, Cheng D, Liu A, Liu J, Liu C, Zhao S, Song J (2016) Cuticular wax accumulation is associated with drought tolerance in wheat near-isogenic lines. Int J Life Sci 7:1–10

    Google Scholar 

  36. Grncarevic M, Radler F (1967) The effect of wax components on cuticular transpiration-model experiments. Planta 75:23–27

    CAS  PubMed  Google Scholar 

  37. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  PubMed  Google Scholar 

  38. Kim KS, Park SH, Kim DK, Jenks MA (2007a) Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. J Plant Physiol 164:1134–1143

    CAS  PubMed  Google Scholar 

  39. Kim KS, Park SH, Kim DK, Jenks MA (2007b) Influence of water deficit on leaf cuticular waxes of soybean (Glycine max L. Merr.). Int J Plant Sci 168:307–316

    CAS  Google Scholar 

  40. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lu S, Joube’s J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151:1918–1929

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Jordaan A, Kruger H (1998) Notes on the cuticular ultrastructure of six xerophytes from Southern Africa. S Afr J Bot 64:82–85

    Google Scholar 

  42. Jumrani K, Bhatia VS (2019) Interactive effect of temperature and water stress on physiological and biochemical processes in soybean. Physiol Mol Biol Plants 25:667–681

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Larsson S, Svenningsson M (1986) Cuticular transpiration and epicuticular lipids of primary leaves of barley (Hordeum vulgare). Physiol Plant 68:13–19

    CAS  Google Scholar 

  44. Lichtenthaler H (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    CAS  Google Scholar 

  45. Lima Neto MC, Silveira JAG, Cerqueira JVA, Cunha JR (2017) Regulation of the photosynthetic electron transport and specific photoprotective mechanisms in Ricinus communis under drought and recovery. Acta Physiol Plant 39:1–12

    CAS  Google Scholar 

  46. Lobato AKS, Oliveira Neto CF, Santos Filho BG, Costa RCL, Cruz FJR, Neves HKB, Lopes MJS (2008) Physiological and biochemical behavior in soybean (Glycine max cv. Sambaiba) plants under water deficit. Aust J Crop Sci 2:25–32

    CAS  Google Scholar 

  47. Medeiros DB, Silva EC, Santos HRB, Pacheco CM, Musser RS, Nogueira RJM (2012) Physiological and biochemical responses to drought stress in Barbados cherry. Braz J Plant Physiol 24:181–192

    CAS  Google Scholar 

  48. Milani M, Nóbrega MBM, Gondim TMS, Andrade FPA, Suassuna ND, Coutinho WM (2007) BRS Energia. Embrapa Algodão, Campina Grande

    Google Scholar 

  49. Mohammadkhani N, Heidari R (2008) Effects of drought stress on soluble proteins in two maize varieties. Turk J Biol 32:23–30

    CAS  Google Scholar 

  50. Moraes PF, de Laat DM, Santos MEAHP, Colombo CA, Kiihl T (2015) Genes differentially expressed in castor bean genotypes (Ricinus communis l.) under water stress induced by peg. Bragantia 74:25–32

    Google Scholar 

  51. Nakano Y, Assada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  52. Ni Y, Guo YJ, Guo YJ, Han L, Tang H, Conyers M (2012) Leaf cuticular waxes and physiological parameters in alfafa leaves as influenced by drought. Photosynthetica 50:458–466

    CAS  Google Scholar 

  53. Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Okunlola GO, Olatunji OA, Akinwale RO, Tariq A, Adelusi AA (2017) Physiological response of the three most cultivated pepper species (Capsicum spp.) in Africa to drought stress imposed at three stages of growth and development. Sci Hortic 224:98–205

    Google Scholar 

  55. Oliveira AFM, Meirelles ST, Salatino A (2003) Epicuticular waxes from caatinga and cerrado species and their efficiency against water loss. An Acad Bras Cienc 75:431–439

    CAS  PubMed  Google Scholar 

  56. O'Toole JC, Cruz RT, Seiber JN (1979) Epicuticular Wax and Cuticular Resistance in Rice. Physiol Plant 47:239–244

    CAS  Google Scholar 

  57. Premachandra GS, Saneoka H, Fujita K, Ogata S (1992) Leaf water relations, osmotic adjustment, cell membrane stability, epicuticular wax load and growth as affected by increasing water deficits in sorghum. J Exp Bot 43:1569–1576

    CAS  Google Scholar 

  58. Racchi ML (2013) Antioxidant defenses in plants with attention to Prunus and Citrus spp. Antioxidants 2:340–369

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Ramel F, Birtic S, Cuiné S, Triantaphylide’s C, Ravanat JL, Havaux M (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158:1267–1278

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Rao DE, Chaitanya KV (2016) Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. Biol Plant 60:1–18

    Google Scholar 

  61. Rasband WS (2012) Image J. US National Institutes of Health Bethesda, Maryland, USA

    Google Scholar 

  62. Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot 52:2023–2032

    CAS  PubMed  Google Scholar 

  63. Saadaoui E, Martín JJ, Tlili N, Cervantes E (2017) Castor bean (Ricinus communis L.): Diversity, seed oil and uses. In: Ahmad P (ed) Oilseed Crops: Yield and Adaptations under Environmental Stress. Wiley-Blackwell, London, pp 19–33

    Google Scholar 

  64. Samdur MY, Manivel P, Jain VK, Chikani BM, Gor HK, Desai S, Misra JB (2003) Genotypic differences and water deficit induced enhancement in epicuticular wax load in peanut. Crop Sci 43:1294–1299

    Google Scholar 

  65. Santos CM, Endres L, Ferreira VM, Silva JV, Rolim EV, Wanderley Filho HCL (2017) Photosynthetic capacity and water use efficiency in Ricinus communis (L.) under drought stress in semi-humid and semi-arid areas. An Acad Bras Cienc 89:3015–3029

    PubMed  Google Scholar 

  66. Sausen TL, Rosa LMG (2010) Growth and carbon assimilation limitations in Ricinus communis (Euphorbiaceae) under soil water stress conditions. Acta Bot Bras 24:648–654

    Google Scholar 

  67. Seo PJ, Lee SB, Suh MC, Park M, Go YS, Park C (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138–1152

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Severino LS, Auld DL (2013) A framework for the study of the growth and development of castor plant. Ind Crops Prod 46:25–38

    Google Scholar 

  69. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26

    Google Scholar 

  70. Schreiber L, Riederer M (1996) Ecophysiology of cuticular transpiration: comparative investigation of cuticular water permeability of plant species from different habitats. Oecologia 107:426–432

    CAS  PubMed  Google Scholar 

  71. Silva MMA, Santos DYAC, Oliveira AFM, Camara TR (2016) Response of Ricinus communis L. to in vitro water stress induced by polyethylene glycol. Plant Growth Regul 78:195–204

    CAS  Google Scholar 

  72. Silva MMA, Santos DYAC, Melo-de-Pinna GF, Camara TR, Oliveira AFM (2017) Chemical composition and ultrastructure of the foliar cuticular wax of two Brazilian cultivars of castor bean (Ricinus communis L.). Ind Crops Prod 95:558–563

    CAS  Google Scholar 

  73. Singh S, Verma A, Dubey VK (2012) Effectivity of anti-oxidative enzymatic system on diminishing the oxidative stress induced by aluminum in chickpea (Cicer arietinum L.) seedlings. Braz J Plant Physiol 24:47–54

    CAS  Google Scholar 

  74. Surendar KK, Devi DD, Ravi I, Jeyakumar P, Velayudham K (2013) Water stress affects plant relative water content, soluble protein, total chlorophyll content and yield of ratoon banana. Int J Hortic 3:96–103

    Google Scholar 

  75. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Breusegem FV, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968

    PubMed  PubMed Central  Google Scholar 

  76. Vermeer CP, Nastold P, Jetter R (2003) Homologous very-long-chain 1,3-alkanediols and 3-hydroxyaldehydes in leaf cuticular waxes of Ricinus communis L. Phytochemistry 62:433–438

    CAS  PubMed  Google Scholar 

  77. Vianna JNS, Pereira MC, Duarte LMG, Wehrmann ME (2012) O papel das oleaginosas em um cenário de mudanças climáticas no semiárido brasileiro. Rev Bras Geo Fís 6:1426–1445

    Google Scholar 

  78. Wang Y, Jin S, Xu Y, Li S, Zhang S, Yuan Z, Li J, Ni Y (2019) Overexpression of BnKCS1-1, BnKCS1-2, and BnCER1-2 promotes cuticular wax production and increases drought tolerance in Brassica napus. Crop J. https://doi.org/10.1016/j.cj.2019.04.006

    Article  Google Scholar 

  79. Zhou X, Linzhi L, Xiang J, Gao G, Xu F, Liu A, Zhang X, Peng Y, Chen X, Wan X (2015) OsGL1-3 is involved in cuticular wax biosynthesis and tolerance to water deficit in rice. PLoS ONE 10:1–18

    Google Scholar 

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Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001. AFMO and DYACS are supported by researcher fellowship of CNPq. We are grateful to Empresa Brasileira de Pesquisa Agropecuária (Embrapa/CNPA), for providing the seeds of castor bean genotypes.

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de Araújo Silva, M.M., Ferreira, L.T., de Vasconcelos, F.M.T. et al. Water Stress-Induced Responses in the Growth, Cuticular Wax Composition, Chloroplast Pigments and Soluble Protein Content, and Redox Metabolism of Two Genotypes of Ricinus communis L.. J Plant Growth Regul 40, 342–352 (2021). https://doi.org/10.1007/s00344-020-10103-6

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Keywords

  • Drought tolerance
  • Oilseeds
  • Oxidative stress
  • Plant cuticle
  • Superoxide dismutase