Skip to main content
SpringerLink
Log in

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.

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

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

    CAS  Google Scholar 

  • 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.

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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  Google Scholar 

  • 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 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

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

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

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

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

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

    CAS  Google Scholar 

  • 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 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

Download references

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.

Author information

Authors and Affiliations

  1. Instituto Federal de Rondônia, Campus Jaru, Jaru, RO, 76890-000, Brazil

    Marina Medeiros de Araújo Silva

  2. Departamento de Fitotecnia e Ciências Ambientais, Universidade Federal da Paraíba, Areia, PB, 58397-000, Brazil

    Lais Tomaz Ferreira & Felipe Matheus Teles de Vasconcelos

  3. Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, PE, 52171-900, Brazil

    Lilia Willadino

  4. Departamento de Química, Universidade Federal Rural de Pernambuco, Recife, PE, 52171-900, Brazil

    Terezinha Rangel Camara

  5. Departamento de Botânica, Universidade de São Paulo, São Paulo, SP, 05508-090, Brazil

    Déborah Yara Alves Cursino dos Santos

  6. Departamento de Botânica, Universidade de Federal de Pernambuco, Recife, PE, 50670-901, Brazil

    Antônio Fernando Morais de Oliveira

Authors
  1. Marina Medeiros de Araújo Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lais Tomaz Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Felipe Matheus Teles de Vasconcelos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lilia Willadino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Terezinha Rangel Camara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Déborah Yara Alves Cursino dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antônio Fernando Morais de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antônio Fernando Morais de Oliveira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-020-10103-6

Keywords

Search

Navigation