Skip to main content

Advertisement

Log in

Antioxidant and photoprotective defenses in response to gradual water stress under low and high irradiance in two Malvaceae tree species used for tropical forest restoration

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

This study provides a mechanistic basis of the tolerance to light and water stress in two tropical tree species of the Malvaceae used for the reforestation in the tropics. G. ulmifolia is more sensitive to high irradiance than C. speciosa . Thus, C. speciosa is more appropriate for the reforestation of degraded areas with potential excess light or water deficit.

Abstract

Reforestation programs in tropics are necessary to mitigate the impacts of climate change, the preservation of biodiversity and for recovery of degraded areas. However, little is known about the abiotic stress tolerance of the major tropical tree species used in reforestation. This study was aimed at evaluating antioxidant defenses and photoprotective pigments against excess light and water deficit in Guazuma ulmifolia Lam. and Ceiba speciosa (A.St.-Hil) Ravenna. Plantlets of 6-month-old were exposed to progressive water deficit by withholding water under high and low irradiance growth conditions and then re-irrigated. G. ulmifolia leaves under high irradiance showed increased photo-oxidative damage, as indicated by a decreased Fv/Fm ratio and 5−12-fold increases in MDA levels, which correlated with a 14-fold increase in SOD activity, a 90 % decrease in POD activity and a 3−4-fold increases in hydrogen peroxide levels. Water deficit combined with high irradiance caused stronger chronic photoinhibition, indicating a synergistic effect that cannot be counterbalanced by antioxidant or photo-protective mechanisms. In contrast, to avoid photo-oxidative damage, C. speciosa enhanced SOD activity, maintained POD and CAT activities, and increased xanthophyll cycle pool size and DPS and β-carotene accumulation. These results indicate that G. ulmifolia is more sensitive to high irradiance than C. speciosa at early stages of development. Thus, C. speciosa is more appropriate for the reforestation of degraded areas with potential excess light or water deficit. In conclusion, this study provides a mechanistic basis of the tolerance abiotic stress in two tropical trees, thereby contributing for management strategies in reforestation projects.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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 Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684

    Article  Google Scholar 

  • Almeida LP, Alvarenga AA, Castro EM, Zanela SM, Vieira CV (2004) Early growth of plants of Cryptocaria aschersoniana Mez. submitted to radiation solar levels. Cienc Rural 34:83–88 (in Portuguese)

    Article  Google Scholar 

  • Amaral JS, Casal S, Torres D, Seabra RM, Oliveira BPP (2005) Simultaneous determination of tocopherols and tocotrienols in hazelnuts by a normal phase liquid chromatographic method. Anal Sci 21:1545–1548

    Article  CAS  PubMed  Google Scholar 

  • Amin B, Mahleghah G, Mahmood HMR, Hossein M (2009) Evaluation of interaction effect of drought stress with ascorbate and salicylic acid on some of physiological and biochemical parameters in Okra (Hibiscus esculentus L.). Res J Biol Sci 4:380–387

    Google Scholar 

  • Angelopoulos K, Dichio B, Xiloyannis C (1996) Inhibition of photosynthesis in olive trees (Olea europaea L.) during water stress and rewatering. J Exp Bot 47:1093–1100

    Article  CAS  Google Scholar 

  • Aquino SD, Cassiolato AMR (2002) Contribution of arbuscular mycorrhizal fungi to the growth of Guazuma ulmifolia in degraded ‘cerrado’ soil. Pesq Agropec Bras 37(12):1819–1823

    Article  Google Scholar 

  • Asensi-Fabado MA, Munné-Bosch S (2010) Vitamins in plants: occurrence, biosynthesis and antioxidant function. Trends Plant Sci 15:582–592

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  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 the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292

    Article  CAS  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beis A, Patakas A (2012) Relative contribution of photoprotection and anti-oxidative mechanisms to differential drought adaptation ability in grapevines. Environ Exp Bot 78:173–183

    Article  CAS  Google Scholar 

  • Berli FJ, Moreno D, Piccoli P, Hespanhol-Viana L, Silva MF, Bressan-Smith R, Cavagnaro JB, Bottini R (2010) Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols. Plant Cell Environ 33:1–10

    CAS  PubMed  Google Scholar 

  • Bianchini E, Medri ME, Pimenta JA, Giloni PC, Kolb RM, Correa GT (2000) Anatomical alterations in plants of Chorisia speciosa A. ST.-Hil. submitted to flooding. Interciencia 25:436–441

    Google Scholar 

  • Blödner C, Skroppa T, Johnsen Ø, Polle A (2005) Freezing tolerance in two Norway spruce (Picea abies [L.] Karst.) progenies is physiologically correlated with drought tolerance. J Plant Physiol 162:549–558

    Article  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  Google Scholar 

  • Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Breugel MV, Hall JS, Craven DJ, Gregoire TG, Park A, Dent DH, Wishnie MH, Mariscal E, Deago J, Ibarra D, Cedeño N, Ashton MS (2011) Early growth and survival of 49 tropical tree species across sites differing in soil fertility and rainfall in Panama. For Ecol Manage 261:1580–1589

    Article  Google Scholar 

  • Carneiro MAC, Siqueira JO, Davide AC, Gomes LJ, Curi N, Vale FR (1996) Mycorrhizal fungi and superphosphate on growth of tropical woody species. Scientia For 50:21–36

    Google Scholar 

  • Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384

    Article  CAS  PubMed  Google Scholar 

  • Chazdon RL, Pearcy RW, Lee DW, Fetcher N (1996) Photosynthetic responses of tropical forest plants to contrasting light environments. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 5–55

    Chapter  Google Scholar 

  • Cortezi DG, Colli S (2011) Effect of flooding and application of plant growth regulators on sprouting of Guazuma ulmifolia (Malvaceae) and Sesbania virgata (Fabaceae). Rev Bras Bot 34:423–430 (in Portuguese)

    Article  Google Scholar 

  • Cubasch U, Wuebbles D, Chen D, Facchini M-C, Frame D, Mahowald N, Winther J-G (2013) Introduction. In: Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin d, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Cambridge University, Cambridge

  • Cuzzuol GRF, Milanez CRD (2012) Morphological and physiological adjustments in juvenile tropical trees under contrasting sunlight irradiance, advances in photosynthesis—fundamental aspects, Najafpour M (ed). doi: 10.5772/28182. Available from: http://www.intechopen.com/books/advances-in-photosynthesis-fundamental-aspects/morphological-and-physiological-adjustments-in-juvenile-tropical-trees-under-contrasting-sunlight-ir

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. CMLS Cell Mol Life Sci 57:779–795

    Article  CAS  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Ann Rev Plant Physiol Plant Mol Biol 42:55–76

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–83

    Article  CAS  PubMed  Google Scholar 

  • Ennahli S, Earl HJ (2005) Physiological limitations to photosynthetic carbon assimilation in cotton under water stress. Crop Sci 45:2374–2382

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212

    Article  Google Scholar 

  • Favaretto VF, Martinez CA, Soriani HH, Furriel RPM (2011) Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions. Environ Exp Bot 70:20–28

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Foyer CH, Descourvières P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase I occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gonçalves JFC, Silva CEM, Guimarães DG (2009) Photosynthesis and water potential of andiroba seedlings submitted to water stress and rewetting. Pesq Agropec Bras 44:8–14 (in Portuguese)

    Article  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidant. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci 96:8762–8767

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hong-Bo S, Xiao-Yan C, Li-Ye C, Xi-Ning Z, Gang W, Yong-Bing Y, Chang-Xing Z, Zan-Min H (2006) Investigation on the relationship of proline with wheat anti-drought under soil water deficits. Colloids Surf B: Biointerfaces 53:113–119

    Article  PubMed  Google Scholar 

  • Huang W, Fu PL, Jiang YJ, Zhang JL, Zhang SB, Hu H, Cao KF (2013) Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest. Tree Physiol 33:211–220

    Article  CAS  PubMed  Google Scholar 

  • Huante P, Ceccon E, Orozco-Segovia A, Sánchez-Coronado ME, Acosta I, Rincón E (2012) The role of arbuscular mycorrhizal fungi on the early stage restoration of seasonally dry tropical forest in Chamela, México. Rev Arvore 36:279–289

    Article  Google Scholar 

  • IPCC (2007) Impacts, adaptation and vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change, Cambridge University, Cambridge

  • Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384:557–560

    Article  CAS  Google Scholar 

  • Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21:1798–1812

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lima JA, Santana DG, Nappo ME (2009) Initial behavior of species in revegetation of the gallery forest in the Mandaguari farm in Indianópolis, MG. R Árvore 33:685–694 (in Portuguese)

    Article  Google Scholar 

  • Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424

    Article  CAS  PubMed  Google Scholar 

  • McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Melotto A, Nicodemo ML, Bocchese RA, Laura VA, Gontijo Neto MM, Schleder DD, Pott A, Silva VP (2009) Survival and initial growing of native tree seedlings in pastures of Central Brazil. R Árvore 33:425–432 (in Portuguese)

    Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Morais RR, Gonçalves JFC, Santos Júnior UM, Dünisch O, Santos ALW (2007) Chloroplastid pigment contents and chlorophyll a fluorescence in Amazonian tropical tree species. R Árvore 31:959–966

    Article  Google Scholar 

  • Moratelli EM, Costa MD, Lovato PE, Santos M, Paulilo MTS (2007) Effect of water and light availability on mycorrhizal colonization and growth of Tabebuia avellanedae Lorentz Griseb. (Bignoniaceae) R Árvore 31(3):555–566 (in Portuguese)

    Article  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed Central  PubMed  Google Scholar 

  • Munné-Bosch S (2005) The role of α-tocopherol in plant stress tolerance. J Plant Physiol 162:743–748

    Article  PubMed  Google Scholar 

  • Munné-Bosch S, Alegre L (2000) Changes in carotenoids, tocopherol and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosimarinus officinalis plants. Planta 210:925–931

    Article  PubMed  Google Scholar 

  • Murgueito E, Calle Z, Uribe F, Calle A, Solorio B (2011) Native trees and shrubs for the productive rehabilitation of tropical cattle ranching lands. For Ecol Manage 261:1654–1663

    Article  Google Scholar 

  • Nicodemo MLF, Porfirio-da-Silva V, Santos PM, Vinholis MMB, Freitas AR, Caputti G (2009) Initial development of tree species in silvopastoral system in southern Brasil. Pesq Flor Bras 60:89–92 (in Portuguese)

    Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  Google Scholar 

  • Nogueira A, Martinez CA, Ferreira LL, Prado CHBA (2004) Photosynthesis and water use efficiency in twenty tropical tree species of differing succession status in a Brazilian reforestation. Photosynthetica 42:351–356

    Article  CAS  Google Scholar 

  • Parry AD, Horgan R (1992) Abscisic acid biosynthesis in roots: I. The identification of potential abscisic acid precursors, and other carotenoids. Planta 187:185–191

    Article  CAS  PubMed  Google Scholar 

  • Pfündel E, Bilger W (1994) Regulation and possible function of the violaxanthin cycle. Photosynth Res 42:89–109

    Article  PubMed  Google Scholar 

  • Portes MT, Damineli DSC, Ribeiro RV, Monteiro JAF, Souza GM (2010) Evidence of higher photosynthetic plasticity in the early successional Guazuma ulmifolia Lam. compared to the late successional Hymenaea courbaril L. grown in contrasting light environments. Braz J Biol 70:75–83

    Article  CAS  PubMed  Google Scholar 

  • Povh JA, Rubin Filho CJ, Mourão KSM, Pinto DD (2005) Morphological and anatomical responses of young plants of Chorisia speciosa A. St. Hil. (Bombacaceae) under flood conditions. Acta Sci Biol Sci 27:195–202 (in Portuguese)

    Article  Google Scholar 

  • Ripullone F, Rivelli AR, Baraldi R, Guarini R, Guerrieri R, Magnani F, Peñuelas J, Raddi S, Borghetti M (2011) Effectiveness of the photochemical reflectance index to track photosynthetic activity over a range of forest tree species and plant water status. Funct Plant Biol 38:177–186

    Article  CAS  Google Scholar 

  • Rodrigues RR, Lima RAF, Gandolfi S, Nave AG (2009) On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic forest. Biol Conserv 142:1242–1251

    Article  Google Scholar 

  • Sampaio MTF, Polo M, Barbosa W (2012) Study of the growth of tree semideciduous species in a riparian area revegetated. R Árvore 36:879–885

    Article  Google Scholar 

  • Scandalios JG (2002) The rise of ROS. Trends Biocheml Sci 27:483–486

    Article  CAS  Google Scholar 

  • Silva EC, Nogueira RJMC, Vale FHA, Melo NF, Araújo FP (2009) Water relations and organic solutes production in four umbu tree (Spondias tuberosa) genotypes under intermittent drought. Braz J Plant Physiol 21:43–53

    Article  Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58

    Article  CAS  Google Scholar 

  • Tadina N, Germ M, Kreft I, Breznik B, Gaberščik A (2007) Effects of water deficit and selenium on common buckwheat (Fagopyrum esculentum Moench.) plants. Photosynthetica 45:472–476

    Article  CAS  Google Scholar 

  • Turner DP, Koerper GJ, Harmon ME, Lee JJ (1995) A carbon budget for forests of the conterminous United States. Ecol Appl 5:421–436

    Article  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • West PC, Gibbs HK, Monfreda C, Wagner J, Barford CC, Carpenter SR, Foley JA (2010) Trading carbon for food: global comparison of carbon stocks vs. crop yields on agricultural land. Proc Natl Acad Sci 107:19645–19648

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wuethrich B (2007) Biodiversity: reconstructing Brazil’s Atlantic rainforest. Science 315:1070–1072

    Article  PubMed  Google Scholar 

  • Yordanov I, Velikova V, Tsonev T (2003) Plant responses to drought and stress tolerance. Bulg J Plant Physiol Special issue:187−206

  • Zangaro W, Nishidate FR, Vandresen J, Andrade G, Nogueira MA (2007) Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. J Trop Ecol 23:53–62

    Article  Google Scholar 

  • Zeraik AE, Souza FS, Fatibello-Filho O, Leite OD (2008) Development of a spot test for peroxidase activity monitoring during a purification procedure. Quim Nova 31:731–734 (in Portuguese)

    Article  CAS  Google Scholar 

  • Zhang J-L, Meng L-Z, Cao K-F (2009) Sustained diurnal photosynthetic depression in uppermost-canopy leaves of four dipterocarp species in the rainy and dry seasons: does photorespiration play a role in photoprotection? Tree Physiol 29:217–228

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Grant 304450/2009-0) to C. A. Martinez. D. R. Contin was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) Graduate Studentships (Grant n˚10422/12-9). D. R. Contin is a CAPES Fellowships (Process n˚10422/12-9). H. H. Soriani was supported by CNPq Graduate Studentships. C. A. Martinez and R. P. M. Furriel are fellow researchers from CNPq.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carlos A. Martinez.

Additional information

Communicated by R. Hampp.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Contin, D.R., Soriani, H.H., Hernández, I. et al. Antioxidant and photoprotective defenses in response to gradual water stress under low and high irradiance in two Malvaceae tree species used for tropical forest restoration. Trees 28, 1705–1722 (2014). https://doi.org/10.1007/s00468-014-1079-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-014-1079-x

Keywords

Navigation