Performance of Hevea brasiliensis under drought conditions on osmoregulation and antioxidant activity through evaluation of vacuolar invertase and reducing sugars
DOI:
https://doi.org/10.14719/pst.2021.8.2.1020Keywords:
carbon metabolism, Rubber tree clones, Drought-recovered, Saccharolytic enzymesAbstract
Rubber tree cultivation is limited in many regions by abiotic factors such as drought. We investigated the biochemical mechanisms responsible for responses to, and recovery from, drought conditions during the establishment phase of four high latex producing rubber tree clones (RRIM600, IAC40, PR255 and GT1). Five-month-old plants were exposed to 32 days of water restriction, followed by 15 days of soil rehydration. Leaf area, as well as their osmolyte accumulations, saccharolytic enzyme activity, and oxidative stress markers, were accompanied. Although clones IAC40 and PR255 responded more precociously to drought conditions, halting leaf expansion before clones GT1 and RRIM600, they demonstrated slow recuperation after reestablishing irrigation. The greater tolerances of clones RRIM600 and GT1 to drought conditions were related to greater vacuolar invertase (VINV) activity in their leaves, which guaranteed more significant accumulations of vacuolar reducing sugars (RS). Similar to RS, glycine betaine accumulations were related to osmoprotection and to reducing oxidative damage (lipidic peroxidation) caused by water deficit conditions. The observed decreases in cytosol neutral invertase (AINV) and cell wall insoluble invertase (CWINV) activities, which resulted in cytosol hexose decreases, may be related to increases in antioxidant enzyme (superoxide dismutase and ascorbate peroxidase) activities in the leaves in response to water deficit conditions. As such, the introduction of specific sugars (RS) and the modulation of key carbon metabolism enzymes, such as VINV, are promising strategies for promoting drought tolerance in rubber tree clones.
Downloads
References
Debaeke P, Bedoussac L, Bonnet C, Bret-Mestries E, Seassau C, Gavaland A, et al. Sunflower crop: environmental-friendly and agroecological. OCL [Internet]. 2016;24(3):304. Available from: https://pdfs.semanticscholar.org/253b/18b55a431ccb1094bca40524709e1b3af451.pdf
Farooq M, Hussain M, Wahid A, Siddique KHM. Drought stress in plants: An overview. In: Aroca R, editor. Plant responses to drought stress: From morphological to molecular features. 2012.
Miyan MA. Droughts in Asian Least Developed Countries: vulnerability and sustainability. (Special Issue: International Geosphere-Biosphere Programme: Asia-Pacific Network for Global Change Research.). Weather Clim Extrem. 2015;7:8-23.
Alexandratos N, Bruinsma J. World agriculture towards 2030/2050. Land use policy. 2012;
Santos JO, Oliveira LEMD, Souza TD, Lopes GM, Coelho VT, Gomes MP. Physiological mechanisms responsible for tolerance to, and recuperation from, drought conditions in four different rubber clones. Ind Crops Prod. 2019;141:111714.
Luiz Furtado E, Da Cunha AR, Alvares CA, Alberto J, Bevenuto Z, Passos JR. Ocorrência de epidemia do mal das folhas em regiões de “escape” do Brasil. Arq Inst Biol. 2015;82:1–6.
Rivano F, Mattos CRR, Cardoso SEA, Martinez M, Cevallos V, Le Guen V, et al. Breeding Hevea brasiliensis for yield, growth and SALB resistance for high disease environments. Industrial Crops and Products. 2013;44:659-70.
Silva CC, Mantello CC, Campos T, Souza LM, Gonçalves PS, Souza AP. Leaf-, panel- and latex-expressed sequenced tags from the rubber tree (Hevea brasiliensis) under cold stressed and suboptimal growing conditions: the development of gene-targeted functional markers for stress response. Mol Breed. 2014;34:1035-53.
Austin D, Rao GG, Rajogopal R, Sanjeeva RP, George MJ, Vijayakumar R, et al. Studies on soil-plant-atmosphere system in Hevea: II. Seasonal effects on water relations and yield. Indian J Nat Rubb Res. 1988;1:45-60.
Ashraf M, Harris PJC. Photosynthesis under stressful environments: An overview. Photosynthetica. 2013;51:163-90.
Krasensky J, Jonak C. Drought, salt and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot. 2012;63:1593–1608.
Sami F, Yusuf M, Faizan M, Faraz A, Hayat S. Role of sugars under abiotic stress Investigation of brassinosteroid mediated abiotic stress tolerance mechanism in crop plants. Artic Plant Physiol Biochem [Internet]. 2016;190:54-61. Available from: http://dx.doi.org/10.1016/j.plaphy.2016.09.005
Bartels D, Sunkar R. Drought and salt tolerance in plants. CRC Crit Rev Plant Sci. 2005;1:23-58.
Kameli A, Lolsel DM. Carbohydrates and water status in wheat plants under water stress. New Phytol. 1993;125:609-14.
Piaskowski JL, Brown D, Campbell KG. Near-infrared calibration of soluble stem carbohydrates for predicting drought tolerance in spring wheat. Agron J. 2016;108:285-93.
Adams HD, Germino MJ, Breshears DD, Barron-Gafford GA, Guardiola-Claramonte M, Zou CB, et al. Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol. 2013;197(4):1142-51.
Sami F, Yusuf M, Faizan M, Faraz A, Hayat S. Role of sugars under abiotic stress. Plant Physiol Biochem. 2016;109:54–61.
Griffiths CA, Paul MJ, Foyer CH. Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochim Biophys Acta-Bioenerg. 2016;1857(10):1715–25.
Liu S, Lan J, Zhou B, Qin Y, Zhou Y, Xiao X, et al. HbNIN2, a cytosolic alkaline/neutral-invertase, is responsible for sucrose catabolism in rubber-producing laticifers of Hevea brasiliensis (para rubber tree). New Phytol. 2015;206(2):709–25.
Nemati F, Ghanati F, Ahmadi Gavlighi H, Sharifi M. Comparison of sucrose metabolism in wheat seedlings during drought stress and subsequent recovery. Biol Plant. 2018;62(3):595-99.
Ruan YL. Sucrose Metabolism: Gateway to Diverse Carbon Use and Sugar Signaling. Annu Rev Plant Biol. 2014;65:33-67.
Gomes MP, Garcia QS. Reactive oxygen species and seed germination. Biologia (Bratisl) [Internet]. 2013;68(3):351–57. Available from: http://link.springer.com/10.2478/s11756-013-0161-y
Everard JD, Loescher WH. Primary products of photosynthesis, sucrose and other soluble carbohydrates. In: Encyclopedia of Applied Plant Sciences. 2016;96–104.
Cavatte PC, Oliveira ÁAG, Morais LE, Martins SCV, Sanglard LMVP, Damatta FM. Could shading reduce the negative impacts of drought on coffee? A morphophysiological analysis. Physiol Plant. 2012;144(2):111-22.
Basu PS, Sharma A, Garg ID, Sukumaran NP. Tuber sink modifies photosynthetic response in potato under water stress. Environ Exp Bot. 1999;42(1):25–39.
Lawlor DW, Cornic G. Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ. 2002;25(2):275-94.
Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F. Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiology. 1999;119(3):1100-99. Available from: https://doi.org/10.1104/pp.119.3.1091
Yang J, Zhang J, Li C, Zhang Z, Ma F, Li M. Response of sugar metabolism in apple leaves subjected to short-term drought stress. Plant Physiol Biochem [Internet]. 2019;141:164–71.
Silva PEM, Cavatte PC, Morais LE, Medina EF, DaMatta FM. The functional divergence of biomass partitioning, carbon gain and water use in Coffea canephora in response to the water supply: Implications for breeding aimed at improving drought tolerance. Environ. Exp. Bot. 2013;87:49-57.
Cavalcante JR, De Cássia CE. Desempenho de cinco clones jovens de seringueira na região do Planalto Ocidental Paulista. Bragantia. 2002;61(3):237-45.
Gonçalves PS, Aguiar ATE, Gouvêa LRL, Souza Gonçalves P, Tosoni EAA, Gouvêa LRL. Expressão fenotípica de clones de seringueira na região noroeste do estado de São Paulo. Bragantia. 2006;65(3):389–98.
Gonçalves PS, Bortoletto N, Sambugaro R, Furtado EL, Bataglia OC, Ortolani AA, Gentil GJ. Desempenho de clones de seringueira de origem amazônica no planalto do Estado de São Paulo. Pesqui. Agropecuária Bras. 2001;36(12):1469–77.
Gonçalves PS, Marques JRB. Clones de seringueira: Influência dos fatores ambientais na produção e recomendação para o plantio. In: Seringueira. Viçosa: EPAMIG; 2008;179–48.
Zanandrea I, Alves JD, Deuner S, Goulart PDFP, Henrique PDC, Silveira NM. Tolerance of Sesbania virgata plants to flooding. Aust J Bot. 2010;57(8):661-69.
Dische Z. General color reactions. Carbohydr Chem. 1962;477–512.
Miller GL. Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal. Chem. 1959;31(3):426-28.
Yemm EW, Cocking EC, Ricketts RE. The determination of amino-acids with ninhydrin. Analyst. 1955;80(948):209-14.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Bio. 1976;72(1-2):248–54.
Grieve CM, Grattan SR. Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil. 1983;70(2):303-07.
Zeng Y, Wu Y, Avigne WT, Koch KE. Rapid repression of Maize Invertases by low oxygen. invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiol. 1999;121(2):599–608.
Cazetta J, Seebauer JR, Bellow F. Sucrose and nitrogen supplies regulate growth of maize kernels. Ann Bot. 1999;84(6):747–54. Available from: https://doi.org/10.1006/anbo.1999.0976
Lowell CA, Tomlinson PT, Koch KE. Sucrose-metabolizing enzymes in transport tissues and adjacent sink structures in developing citrus fruit. Plant Physiol. 1989;90(4):1394–1402. Available from: https://doi.org/10.1104/pp.90.4.1394
Giannopolitis CN, Ries SK. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 1977;59(2):309-14.Available from: https://doi.org/10.1104/pp.59.2.309
Havir EA, McHale NA. Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol. 1987;84(2):450-55. Available from https://doi.org/ 10.1104/pp.84.2.450
Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981;22(5):867–80. Available from: https://doi.org/10.1093/oxfordjournals.pcp.a076232
Buege JA, Aust SD. [30] Microsomal lipid peroxidation. Methods Enzymol. 1978;52:302–10. Available from: https://doi.org/10.1016/S0076-6879(78)52032-6
Shapiro SS, Wilk MB. An analysis of variance test for normality (complete samples). Biometrika. 1965;523(3):591-611. Available from: https://doi.org/10.1093/biomet/52.3-4.591
Bergman ET, Roediger HL. Can Bartlett’s repeated reproduction experiments be replicated?. Mem. Cogn. 199;27:937–47. Available from: https://doi.org/10.3758/BF03201224
R core team. R: A Language and environment for statistical computing. R Foundation for Statistical Computing. 2019.
Ferreira EB, Cavalcanti PP, Nogueira DA. ExpDes.pt: pacote experimental designs (Portuguese). 2018. Available from: https://cran.r-project.org/package=ExpDes.pt
Ginestet, C. ggplot2: Elegant graphics for data analysis. Journal of the Royal Statistical Society. 2011;174:245-46. Available from: https://doi.org/10.1111/j.1467-985X.2010.00676_9.x
Groth, D., Hartmann, S., Klie, S., Selbig, J. Principal components analysis. In: Reisfeld B., Mayeno A. (eds) Computational Toxicology. Methods in Molecular Biology (Methods and Protocols) Humana Press, Totowa. 2013;930:527-47. Available from: https://doi.org/10.1007/978-1-62703-059-5_22
Kassambara A, Mundt F. Package “factoextra” for R: Extract and visualize the results of multivariate data analyses. R Packag version. 2017;1(5):337-54.
Tang Y, Horikoshi M, Li W. Ggfortify: Unified interface to visualize statistical results of popular R packages. The R Journal. 2016;8(2):474.
Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A. Plant sugars are crucial players in the oxidative challenge during abiotic stress: Extending the traditional concept. Plant Cell Environ. 2013;36(7):1242-55. Available from: http//dx.doi.org/ 10.1111/pce.12061
Trouverie J, Chateau-Joubert S, Thévenot C, Jacquemot MP, Prioul JL. Regulation of vacuolar invertase by abscisic acid or glucose in leaves and roots from maize plantlets. Planta. 2004;219(5):894-905. Available from: https://doi.org/10.1007/s00425-004-1289-3
Devakumar A. Photosynthesis in mature trees of Hevea brasiliensis experiencing drought and cold stresses concomitant with high light in the Field. Indian J Nat Rubber Res. 2002;15:1–13.
Wellstein C, Poschlod P, Gohlke A, Chelli S, Campetella G, Rosbakh S, et al. Effects of extreme drought on specific leaf area of grassland species: A meta-analysis of experimental studies in temperate and sub-Mediterranean systems. Glob Chang Biol. 2017;23(6):2473-81. Available from: https://doi.org/10.1111/gcb.13662
Bonfig KB, Gabler A, Simon UK, Luschin-Ebengreuth N, Hatz M, Berger S, Muhammad N, Zeier J, Sinha AK, Roitsch T. Post-translational derepression of invertase activity in source leaves via down-regulation of invertase inhibitor expression is part of the plant defense response. Mol Plant. 2010;3(6):1037-48. Available from: https://doi.org/10.1093/mp/ssq053
Roitsch T, González MC. Function and regulation of plant invertases: Sweet sensations. Trends in Plant Science 2004;9(12):606–13. Available from https://doi.org/10.1016/j.tplants.2004.10.009
Geigenberger P, Stitt M. Sucrose synthase catalyses a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta. 1993;189(3):329-39. Available from: https://doi.org/10.1007/BF00194429
Skirycz A, Inzé D. More from less: Plant growth under limited water. Current Opinion in Biotechnology. 2010;21(2):197-203. Available from: https://doi.org/10.1016/j.copbio.2010.03.002
Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, et al. Water deficits uncouple growth from photosynthesis, increase C content and modify the relationships between C and growth in sink organs. J Exp Bot. 2011;62(6):1715-29. Available from: https://doi.org/10.1093/jxb/erq438
Parvanova D, Popova A, Zaharieva I, Lambrev P, Konstantinova T, Taneva S, et al. Low temperature tolerance of tobacco plants transformed to accumulate proline, fructans or glycine betaine. Variable chlorophyll fluorescence evidence. Photosynthetica. 2004;42(2):179-85. Available from: https://doi.org/10.1023/B:PHOT.0000040588.31318.0f
Quan R, Shang M, Zhang H, Zhao Y, Zhang J. Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol J. 2004;2(6):477–86. Available from: https://doi.org/10.1111/j.1467-7652.2004.00093.x
He C, Zhang W, Gao Q, Yang A, Hu X, Zhang J. Enhancement of drought resistance and biomass by increasing the amount of glycine betaine in wheat seedlings. Euphytica. 2011;177(2):151–67. Available from: https://doi.org/10.1007/s10681-010-0263-3
Wang M, Tang JC. Research of antibiotics pollution in soil environments and its ecological toxicity. J Agric Environ Sci. 2010;29:261–66.
Giri J. Glycine betaine and abiotic stress tolerance in plants. Plant Signal Behav. 2011;6(11):1746-51. Available from: https://doi.org/10.4161/psb.6.11.17801
Van den Ende W, Valluru R. Sucrose, sucrosyl oligosaccharides and oxidative stress: scavenging and salvaging? J Exp Bot. 2009;60(1):9–18. Available from: https://doi.org/10.1093/jxb/ern297
Peshev D, Vergauwen R, Moglia A, Hideg E, Van den Ende W. Towards understanding vacuolar antioxidant mechanisms: a role for fructans? J Exp Bot. 2013;64(4):1025–38. Available from: https://doi.org/10.1093/jxb/ers377
Valluru R, Van Den Ende W. Plant fructans in stress environments: Emerging concepts and future prospects. Journal of Experimental Botany. 2008;59(11):2095-16. Available from: https://doi.org/10.1093/jxb/ern164
Tognetti JA, Pontis HG, Martínez-Noël GMA. Sucrose signaling in plants: A world yet to be explored. Plant Signaling and Behavior. 2013;8(3):e23316. Available from: https://doi.org/10.4161/psb.23316
Wind J, Smeekens S, Hanson J. Sucrose: Metabolite and signaling molecule. Phytochemistry. 2010;71:1610–14. Available from: https://doi.org/10.1016/j.phytochem.2010.07.007
Xiang L, Li Y, Rolland F, Van den Ende W. Neutral invertase, hexokinase and mitochondrial ROS homeostasis: emerging links between sugar metabolism, sugar signaling and ascorbate synthesis. Plant Signal Behav. 2011;6(10):1567–73. Available from: https://doi.org/10.4161/psb.6.10.17036
Storr T, Hall JL. The effect of infection by Erysiphe pisi DC on acid and alkaline invertase activities and aspects of starch biochemistry in leaves of Pisum sativum L. New Phytol. 1992;121(4):535–43. Available from: https://doi.org/10.1111/j.1469-8137.1992.tb01123.x
Essmann J, Bones P, Weis E, Scharte J. Leaf carbohydrate metabolism during defense. Plant Signal Behav. 2008;3(10):885–87. Available from: https://doi.org/10.4161/psb.3.10.6501
Park J, Kim S, Choi E, Auh C-K, Park J-B, Kim D, Chung YJ, Lee TK, Lee S. Altered invertase activities of symptomatic tissues on Beet severe curly top virus (BSCTV) infected Arabidopsis thaliana. J Plant Res. 2013;126(5):743-52. Available from: https://10.1007/s10265-013-0562-6
Tripathy BC, Oelmüller R. Reactive oxygen species generation and signaling in plants. Plant Signal Behav. 2012;7(12):1621–33. Available from: https://doi.org/10.4161/psb.22455
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Jacqueline Santos, Luiz Edson Oliveira, Victor Tadeu Coelho, Guilherme Lopes, Thaiara Souza, Antonio Carlos Porto, Jean Lira, Rafaela Massote, Camila Rocha, Marcelo Pedrosa Gomes
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright and Licence details of published articles
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
Open Access Policy
Plant Science Today is an open access journal. There is no registration required to read any article. All published articles are distributed under the terms of the Creative Commons Attribution License (CC Attribution 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited (https://creativecommons.org/licenses/by/4.0/). Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
