Abstract
Ricinus communis is one of the major commercial non-edible oilseed crops grown in semiarid and arid environments worldwide and is reported as a drought tolerant species. Surprisingly, little is known about the mechanisms achieving this tolerance, especially in relation to photoprotection. The aim of this study was to analyze the association of the regulation of the photosynthetic electron transport and photoprotective mechanisms with drought tolerance in R. communis. Drought induced decreases in the relative water content, water potential and growth in R. communis exposed to 9 days of drought. After 6 days of rehydration, these parameters were completely recovered, demonstrating a potential of drought tolerance in this species. In addition, drought inhibited photosynthesis by stomatal and metabolic limitations (V cmax, J max, and Rubisco activity), with partial recovery after rehydration. Leaves displayed transient photoinhibition after 6 days of drought, which was completely recovered after 6 days of dehydration. The effective quantum yields and the electron transport rates of PSII and PSI were modulated to face drought avoiding the excess energy produced by decreases in CO2 assimilation. NPQ was increased during drought, and it was maintained higher than control after the recovery treatment. In addition, the estimated cyclic electron flow was induced under drought and decreased after recovery. Photorespiration was also increased under drought and maintained at higher levels after the recovery treatment. Furthermore, antioxidative enzymes activities (SOD, APX, and CAT) were increased under drought to avoid ROS harmful effects. Altogether, we clearly showed that the modulation of photoprotective mechanisms and antioxidant enzymes are crucial to this species under drought. The implication of these strikingly strategies to drought tolerance is discussed in relation to agricultural and natural systems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- Ψ w :
-
Water potential
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- CEF:
-
Cyclic electron flow
- DM:
-
Dry matter
- FM:
-
Fresh matter
- GO:
-
Glycolate oxidase
- LEF:
-
Linear electron flow
- PET:
-
Photosynthetic electron transport
- PPFD:
-
Photosynthetic photon flux density
- P R :
-
Photorespiration
- ROS:
-
Reactive oxygen species
- RuBP:
-
Ribulose 1,5 bisphosphate
- RWC:
-
Relative water content
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- SOD:
-
Superoxide dismutase
- TBARS:
-
Thiobarbituric acid reactive substances
- VPD:
-
Vapor pressure deficit
References
Asada K (2006) Production and scavenging of reactive oxygen species in Chloroplasts and their functions. Plant Physiol 141:391–396. doi:10.1104/pp.106.082040
Babita M, Maheswari M, Rao LM, Shanker AK, Rao DG (2010) Osmotic adjustment, drought tolerance and yield in castor (Ricinus communis L.) hybrids. Environ Exp Bot 69:243–249. doi:10.1016/j.envexpbot.2010.05.006
Bagard M, Le Thiec D, Delacote E, Hasenfratz-Sauder M-P, Banvoy J, Gérard J, Dizengremel P, Jolivet Y (2008) Ozone-induced changes in photosynthesis and photorespiration of hybrid poplar in relation to the developmental stage of the leaves. Physiol Plant 134:559–574. doi:10.1111/j.1399-3054.2008.01160.x
Baker AL, Tolbert NE (1966) Glycolate oxidase (ferredoxin—containing form). Methods Enzymol 9:339–340
Ballottari M, Alcocer MJP, D’Andrea C, Viola D, Ahn TK, Petrozza A, Polli D, Fleming GR, Cerullo G, Bassi R (2014) Regulation of photosystem I light harvesting by zeaxanthin. Proc Natl Acad Sci USA 111:E2431–E2438. doi:10.1073/pnas.1404377111
Barbour MM, Buckley TN (2007) The stomatal response to evaporative demand persists at night in Ricinus communis plants with high nocturnal conductance. Plant Cell Environ 30:711–721. doi:10.1111/j.1365-3040.2007.01658.x
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot. doi:10.1093/aob/mcf118
Bonifacio A, Martins MO, Ribeiro CW, Fontenele AV, Carvalho FEL, Margis-Pinheiro M, Silveira JA (2011) Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress. Plant Cell Environ. doi:10.1111/j.1365-3040.2011.02366.x
Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416. doi:10.1104/pp.59.3.411
Busch FA (2013) Current methods for estimating the rate of photorespiration in leaves. Plant Biol (Stuttg) 15:648–655. doi:10.1111/j.1438-8677.2012.00694.x
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. doi:10.1111/j.1399-3054.1991.tb00121.x
Carvalho FEL, Ware MA, Ruban AV (2015) Quantifying the dynamics of light tolerance in Arabidopsis plants during ontogenesis. Plant Cell Environ 38:2603–2617. doi:10.1111/pce.12574
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. doi:10.1093/aob/mcn125
Dai Z, Edwards GE, Ku MSB (1992) Control of photosynthesis and stomatal conductance in Ricinus communis L. (Castor Bean) by leaf to air vapor pressure deficit. Plant Physiol 99:1426–1434. doi:10.1104/pp.99.4.1426
Demmig-Adams B, Adams WW (1993) The xanthophyll cycle, protein turnover, and the high light tolerance of sun-acclimated leaves. Plant Physiol 103:1413–1420
Finazzi G, Johnson GN, Dallosto L, Dallosto L, Joliot P, Wollman F-A, Bassi R (2004) A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc Natl Acad Sci USA 101:12375–12380. doi:10.1073/pnas.0404798101
Flexas J (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189. doi:10.1093/aob/mcf027
Flexas J, Escalona JM, Medrano H (1999) Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines. Plant Cell Environ 22:39–48. doi:10.1046/j.1365-3040.1999.00371.x
Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298. doi:10.1111/j.1365-3040.2007.01700.x
Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84. doi:10.1016/j.plantsci.2012.05.009
Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484. doi:10.1146/annurev.arplant.043008.091948
Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661. doi:10.1093/jxb/ers013
Galmés J, Ribas-Carbó M, Medrano H, Flexas J (2011) Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress. J Exp Bot 62:653–665. doi:10.1093/jxb/erq303
Giannopolotis CN, Ries SK (1977) Superoxide dismutases: occurrence in higher plants. Plant Physiol 59:309–314
Goh C-H, Ko S-M, Koh S, Kim Y-J, Bae H-J (2011) Photosynthesis and environments: photoinhibition and repair mechanisms in plants. J Plant Biol. doi:10.1007/s12374-011-9195-2
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. doi:10.1104/pp.84.2.450
Hoagland DR, Arnon DJ (1950) The water-culture method for growing plants without soil. Circular. In: California Agricultural Experiment Station, vol 347. 2nd edn
Johnson GN (2011) Reprint of: physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:906–911. doi:10.1016/j.bbabio.2011.05.008
Johnson MP, Zia A, Ruban AV (2011) Elevated ΔpH restores rapidly reversible photoprotective energy dissipation in Arabidopsis chloroplasts deficient in lutein and xanthophyll cycle activity. Planta. doi:10.1007/s00425-011-1502-0
Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322. doi:10.1073/pnas.1110189108
Joliot P, Joliot A (2005) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102:4913–4918. doi:10.1073/pnas.0501268102
Kangasjärvi S, Neukermans J, Li S, Aro E-M, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636. doi:10.1093/jxb/err402
Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta. doi:10.1007/BF00194461
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395. doi:10.1038/35000131
Lichtenthaler H, Wellburn A (1983) Determinations of total carotenoids and chlorophylls b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. doi:10.1042/bst0110591
Lieth JH, Reynolds JF (1987) The nonrectangular hyperbola as a photosynthetic light response model: geometrical interpretation and estimation of the parameter—omega. Photosynthetica 21:363–366
Lima Neto MCL, Lobo AKM, Martins MO, Fontenele AV, Silveira JAG (2014) Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas. J Plant Physiol 171(1):23–30
Lima Neto MC, Martins MO, Ferreira-Silva SL, Silveira JAG (2015) Jatropha curcas and Ricinus communis display contrasting photosynthetic mechanisms in response to environmental conditions. Sci Agric 72:269
Maurino VG, Peterhansel C (2010) Photorespiration: current status and approaches for metabolic engineering. Curr Opin Plant Biol 13:249–256. doi:10.1016/j.pbi.2010.01.006
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought : why do some plants survive while others succumb to drought? New Phytol. doi:10.1111/j.1469-8137.2008.02436.x
Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92. doi:10.1104/pp.110.168831
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbato specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749. doi:10.1016/j.bbabio.2006.05.013
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. doi:10.1104/pp.113.233478
Ogbaga CC, Stepien P, Johnson GN (2014) Sorghum (Sorghum bicolor) varieties adopt strongly contrasting strategies in response to drought. Physiol Plant. doi:10.1111/ppl.12196
Pérez-Torres E, Bravo LA, Corcuera LJ, Johnson GN (2007) Is electron transport to oxygen an important mechanism in photoprotection? Contrasting responses from Antarctic vascular plants. Physiol Plant 130:185–194. doi:10.1111/j.1399-3054.2007.00899.x
Peterhänsel C, Maurino VG (2010) Photorespiration redesigned. Plant Physiol 155:49–55. doi:10.1104/pp.110.165019
Reid CD, Tissue DT, Fiscus EL, Strain BR (1997) Comparison of spectrophotometric and radioisotopic methods for the assay of Rubisco in ozone-treated plants. Physiol Plant 101:398–404. doi:10.1034/j.1399-3054.1997.1010221.x
Ristic Z, Momcilovic I, Bukovnik U, Prasad PVV, Fu J, Deridder BP, Elthon TE, Mladenov N (2009) Rubisco activase and wheat productivity under heat-stress conditions. J Exp Bot 60:4003–4014. doi:10.1093/jxb/erp241
Ruban AV (2016) Non-photochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protection against photodamage. Plant Physiol. doi:10.1104/pp.15.01935
Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. doi:10.1111/j.1365-3040.2007.01675.x
Sage RF, Way DA, Kubien DS (2009) Rubisco, Rubisco activase, and global climate change. Rev Lit Arts Am 59:1581–1595. doi:10.1093/jxb/ern053
Saroussi SI, Wittkopp TM, Grossman AR (2016) The type II NADPH dehydrogenase facilitates cyclic electron flow, energy dependent quenching and chlororespiratory metabolism during acclimation of Chlamydomonas reinhardtii to nitrogen deprivation. Plant Physiol. doi:10.1104/pp.15.02014
Scholander (1960) Sap pressure in vascular plants. Science 148:339–349
Sejima T, Hanawa H, Shimakawa G, Takagi D, Suzuki Y (2016) Post-illumination transient O2-uptake is driven by photorespiration in tobacco leaves. Physiol Plant. doi:10.1111/ppl.12388
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C(3) leaves. Plant Cell Environ 30:1035–1040. doi:10.1111/j.1365-3040.2007.01710.x
Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165. doi:10.1104/pp.108.132407
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270. doi:10.1111/j.1365-3040.2011.02336.x
Takagi D, Hashiguchi M, Sejima T, Makino A, Miyake C (2016) Photorespiration provides the chance of cyclic electron flow to operate for the redox-regulation of P700 in photosynthetic electron transport system of sunflower leaves. Photosynth Res. doi:10.1007/s11120-016-0267-5
Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. doi:10.1016/j.tplants.2008.01.005
Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A (2011) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J 68:966–976. doi:10.1111/j.1365-313X.2011.04747.x
Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6:20147. doi:10.1038/srep20147
Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP (2009) High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiol 149:195–204. doi:10.1104/pp.108.128439
Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546. doi:10.1007/s11120-013-9885-3
Zivcak M, Kalaji HM, Shao H-B, Olsovska K, Brestic M (2014) Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress. J Photochem Photobiol B 137:107–115. doi:10.1016/j.jphotobiol.2014.01.007
Acknowledgements
We are grateful to CNPq (Project 445842/2014-8) and INCTsal-CNPQ/MCTi for financial support and EMPRABA-Cotton by kindly provide the seeds.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by M. Garstka.
Rights and permissions
About this article
Cite this article
Lima Neto, M.C., Silveira, J.A.G., Cerqueira, J.V.A. et al. Regulation of the photosynthetic electron transport and specific photoprotective mechanisms in Ricinus communis under drought and recovery. Acta Physiol Plant 39, 183 (2017). https://doi.org/10.1007/s11738-017-2483-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2483-9