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Photosynthetic acclimation to drought stress in Agave salmiana Otto ex Salm-Dyck seedlings is largely dependent on thermal dissipation and enhanced electron flux to photosystem I

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Abstract

Agave salmiana Otto ex Salm-Dyck, a crassulacean acid metabolism plant that is adapted to water-limited environments, has great potential for bioenergy production. However, drought stress decreases the requirement for light energy, and if the amount of incident light exceeds energy consumption, the photosynthetic apparatus can be injured, thereby limiting plant growth. The objective of this study was to evaluate the effects of drought and re-watering on the photosynthetic efficiency of A. salmiana seedlings. The leaf relative water content and leaf water potential decreased to 39.6 % and −1.1 MPa, respectively, over 115 days of water withholding and recovered after re-watering. Drought caused a direct effect on photosystem II (PSII) photochemistry in light-acclimated leaves, as indicated by a decrease in the photosynthetic electron transport rate. Additionally, down-regulation of photochemical activity occurred mainly through the inactivation of PSII reaction centres and an increased thermal dissipation capacity of the leaves. Prompt fluorescence kinetics also showed a larger pool of terminal electron acceptors in photosystem I (PSI) as well as an increase in some JIP-test parameters compared to controls, reflecting an enhanced efficiency and specific fluxes for electron transport from the plastoquinone pool to the PSI terminal acceptors. All the above parameters showed similar levels after re-watering. These results suggest that the thermal dissipation of excess energy and the increased energy conservation from photons absorbed by PSII to the reduction of PSI end acceptors may be an important acclimation mechanism to protect the photosynthetic apparatus from over-excitation in Agave plants.

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Abbreviations

Chl:

Chlorophyll

ETR:

Electron transport rate

NPQ:

Non-photochemical quenching

OEC:

Oxygen evolving complex

OJIP transient:

Fast (seconds) Chl a fluorescence induction curve where O is for the minimum initial fluorescence, J and I are inflections and P is for peak

PAM:

Pulse amplitude modulation

PAR:

Photosynthetic active radiation

PSI:

Photosystem I

PSII:

Photosystem II

PQ:

Oxidised plastoquinone

QA :

Primary quinone electron acceptor of PSII

RC:

Reaction centre

SWC:

Relative soil water content

ΨL :

Leaf water potential

References

  • Adamski JM, Peters JA, Daniloski R, Bacarin MA (2011) Excess iron-induced changes in the photosynthetic characteristics of sweet potato. J Plant Physiol 168:2056–2062

    Article  PubMed  CAS  Google Scholar 

  • Antal TK, Kolacheva A, Maslakov A, Riznichenko GY, Krendeleva TE, Rubin AB (2013) Study of the effect of reducing conditions on the initial chlorophyll fluorescence rise in the green microalgae Chlamydomonas reinhardtii. Photosynth Res 114:143–154

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125

    Article  PubMed  CAS  Google Scholar 

  • Borland AM, Griffiths H, Hartwell J, Smith AC (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. J Exp Bot 60:2879–2896

    Article  PubMed  CAS  Google Scholar 

  • Borland AM, Zambrano VAB, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytol 191:619–633

    Article  PubMed  CAS  Google Scholar 

  • Broetto F, Duarte HM, Lüttge U (2007) Responses of chlorophyll fluorescence parameters of the facultative halophyte and C3-CAM intermediate species Mesembryanthemum crystallinum to salinity and high irradiance stress. J Plant Physiol 164:904–912

    Article  PubMed  CAS  Google Scholar 

  • Ceppi MG, Oukkaroum A, Çiçek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288

    Article  PubMed  CAS  Google Scholar 

  • Ceusters J, Borland AM, Londers E, Verdoodt V, Godts C, De Proft MP (2009) Differential usage of storage carbohydrates in the CAM bromeliad Aechmea ‘Maya’ during acclimation to drought and recovery from dehydration. Physiol Plant 135:174–184

    Article  PubMed  CAS  Google Scholar 

  • Chou Y, Polansky AM, Mason RL (1998) Transforming non-normal data to normality in statistical process control. J Qual Technol 30:133–141

    Google Scholar 

  • Ehleringer J (1981) Leaf absorptances of Mohave and Sonoran desert plants. Oecologia 49:366–370

    Article  Google Scholar 

  • Flexas J, Barón M, Bota J, Ducruet J-M, Gallé A, Galmés J, Jiménez M, Pou A, Ribas-Carbó M, Sajnani C, Tomàs M, Medrano H (2009) Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandierix, V. rupestris). J Exp Bot 60:2361–2377

    Article  PubMed  CAS  Google Scholar 

  • Fukuyama K (2004) Structure and function of plant-type ferredoxins. Photosynth Res 81:289–301

    Article  PubMed  CAS  Google Scholar 

  • Garcia MA (2002) Distribution of Agave (Agavaceae) in Mexico. Cactus Succul J 74:177–187

    Google Scholar 

  • García-Moya E, Romero-Manzanares A, Nobel PS (2011) Highlights for Agave productivity. GCB Bioenergy 3:4–14

    Article  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114

    Article  PubMed  CAS  Google Scholar 

  • Goltsev V, Zaharieva I, Chemev P, Kouzmanova M, Kalaji HM, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. BBA-Bioenergetics 1817:1490–1498

    Article  PubMed  CAS  Google Scholar 

  • Herppich WB, Peckmann K (1997) Responses of gas exchange, photosynthesis, nocturnal acid accumulation and water relations of Aptenia cordifolia to short-term drought and rewatering. J Plant Physiol 150:467–474

    Article  CAS  Google Scholar 

  • Herppich WB, Peckmann K (2000) Influence of drought on mitochondrial activity, photosynthesis, nocturnal acid accumulation and water relations in the CAM plants Prenia sladeniana (ME-type) and Crassula lycopodioides (PEPC-type). Ann Bot 86:611–620

    Article  CAS  Google Scholar 

  • Herppich WB, Midgley GF, Herppich M, Tuffers A, Veste M, von Willert DJ (1998) Interactive effect of photon fluence rates and drought on CAM-cycling in Delosperma tradescantoides (Mesembryanthemaceae). Physiol Plant 102:148–154

    Article  CAS  Google Scholar 

  • Jiang HX, Chen LS, Zheng JG, Han S, Tang N, Smith BR (2008) Aluminum-induced effects on photosystem II photochemistry in Citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863–1871

    Article  PubMed  CAS  Google Scholar 

  • Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. BBA-Bioenergetics 1807:384–389

    Article  PubMed  CAS  Google Scholar 

  • Krüger TPJ, Ilioaia C, Johnson MP, Ruban AV, Papagiannakis E, Horton P, van Grondelle R (2012) Controlled disorder in plant light-harvesting complex II explains its photoprotective role. Biophys J 102:2669–2676

    Article  PubMed  PubMed Central  Google Scholar 

  • Lazár D (2009) Modelling of light-induced chlorophyll a fluorescence rise (O–J–I–P transient) and changes in 820 nm-transmittance signal of photosynthesis. Photosynthetica 47:483–498

    Article  Google Scholar 

  • Lee HSJ, Lüttge U, Medina E, Smith JAC, Cram WJ, Diaz M, Griffiths H, Popp M, Schäfer C, Stimmel K-H, Thonke B (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela III. Bromelia humilis Jacq. A terrestrial CAM bromeliad. New Phytol 111:253–271

    Article  CAS  Google Scholar 

  • Lüttge U (1990) Nocturnal citrate accumulation and its response to environmental stress in the CAM plant Kalanchoë pinnata (Lam.) Pers. Plant Cell Environ 13:977–982

    Article  Google Scholar 

  • Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93:629–652

    Article  PubMed  Google Scholar 

  • Makarov SS, Grachev EA, Antal TK (2012) Mathematical modeling of photosynthetic electron transport chain considering spatial heterogeneity of the thylakoid membrane. Math Biol Bioinform 7:508–528

    CAS  Google Scholar 

  • Matiz A, Mioto PT, Mayorga AY, freschi L, Mercier H (2013) CAM photosynthesis in Bromeliads and Agaves: what can we learn from these plants? In: Zvy Dubinsky (ed) Photosynthesis, ISBN: 978-953-51-1161-0, InTech. doi:10.5772/56219. Available from: http://www.intechopen.com/books/photosynthesis/cam-photosynthesis-in-bromeliads-and-agaves-what-can-we-learn-from-these-plants-

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Michalowski CB, Olsen SW, Piepenbrock M, Schmitt JM, Bohnert HJ (1989) Time course of mRNA induction elicited by salt stress in the common ice plant (Mesembryanthemum crystallinum). Plant Physiol 89:811–816

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Munday JC Jr, Govindjee (1969) Light-induced changes in the fluorescence yield of chlorophyll a in vivo III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:1–21

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Munekage Y, Shinakai T (2005) Cyclic electron transport through photosystem I. Plant Biotechnol 22:361–369

    Article  CAS  Google Scholar 

  • Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314

    Article  PubMed  CAS  Google Scholar 

  • Nobel PS (1991) Achievable productivities of CAM plants: basis for high values compared with C3 and C4 plants. New Phytol 119:183–205

    Article  CAS  Google Scholar 

  • Nobel PS (1996) High productivity of certain agronomic CAM species. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Springer, Berlin, pp 255–265

    Chapter  Google Scholar 

  • Nobel PS (2010) Desert wisdom/agaves and cacti: CO2, water, climate change. iUniverse, New York

    Google Scholar 

  • Oukarroum A, Madidi SE, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and rewatering. Environ Exp Bot 60:438–446

    Article  CAS  Google Scholar 

  • Oukarroum A, Schansker G, Strasser RJ (2009) Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plant 137:188–199

    Article  PubMed  CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Kluwer (now Springer), Dordrecht

  • Papageorgiou GC, Govindjee (2011) Photosystem II fluorescence: slow changes—scaling from the past. J Photochem Photobiol B 104:258–270

    Article  PubMed  CAS  Google Scholar 

  • Patel A, Ting IP (1987) Relationship between respiration and CAM-cycling in Peperomia camptotricha. Plant Physiol 84:640–642

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pieters AJ, Tezara W, Herrera A (2003) Operation of the xanthophyll cycle and degradation of D1 protein in the inducible CAM plant, Talinum triangulare, under water deficit. Ann Bot 92:393–399

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficient and simultaneous equations for assaying chlorophyll a and chlorophyll b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA-Bioenergetics 975:384–394

    Article  CAS  Google Scholar 

  • Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104

    Article  PubMed  CAS  Google Scholar 

  • Rayder L, Ting IP (1983) CAM-idling in Hoya carnosa (Asclepiadaceae). Photosynth Res 4:203–211

    Article  CAS  Google Scholar 

  • Redillas MCFR, Strasser RJ, Jeong JS, Kim YS, Kim J-K (2011) The use of JIP test to evaluate drought tolerance of transgenic rice overexpressing OsNAC10. Plant Biotechnol Rep 5:169–175

    Article  Google Scholar 

  • Rochaix JD (2011) Regulation of photosynthetic electron transport. BBA-Bioenergetics 1807:375–383

    Article  PubMed  CAS  Google Scholar 

  • Schansker G, Tóth SZ, Strasser RJ (2005) Methyl viologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. BBA-Bioenergetics 1706:250–261

    Article  PubMed  CAS  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  PubMed  CAS  Google Scholar 

  • Smith JAC, Lüttge U (1985) Day-night changes in leaf water relations associated with the rhythm of crassulacean acid metabolism in Kalanchoë daigremontiana. Planta 163:272–282

    Article  PubMed  CAS  Google Scholar 

  • Stirbet A (2013) Excitonic connectivity between photosystem II units: what is it, and how to measure it? Photosynth Res 116:189–214

    Article  PubMed  CAS  Google Scholar 

  • Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B 104:236–257

    Article  PubMed  CAS  Google Scholar 

  • Strasser RJ, Stirbet AD (1998) Heterogeneity of photosystem II probed by the numerically simulated chlorophyll a fluorescence rise (O–J–I–P). Math Comput Simul 48:3–9

    Article  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer Press, Netherlands, pp 321–362

  • Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. BBA-Bioenergetics 1797:1313–1326

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tardieu F (2012) Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J Exp Bot 63:25–31

    Article  PubMed  CAS  Google Scholar 

  • Ting IP (1985) Crassulacean acid metabolism. Annu Rev Plant Physiol 36:595–622

    Article  CAS  Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants’ vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, Berlin, pp 679–703

    Google Scholar 

  • van Heerden PDR, Swanepoel JW, Kruger GHJ (2007) Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation. Environ Exp Bot 61:124–136

    Article  Google Scholar 

  • Wilhelm C, Selmar D (2011) Energy dissipation is an essential mechanism to sustain the viability of plants: the physiological limits of improved photosynthesis. J Plant Physiol 168:79–87

    Article  PubMed  CAS  Google Scholar 

  • Winter K, Garcia M, Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë and Opuntia. J Exp Bot 59:1829–1840

    Article  PubMed  CAS  Google Scholar 

  • Yan K, Chen P, Shao H, Shao C, Zhao S, Brestic M (2013) Dissection of photosynthetic electron transport process in sweet sorghum under heat stress. PLoS One 8:e62100. doi:10.1371/journal.pone.0062100

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimili-Michael M, Govindjee, Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. BBA-Bioenergetics 1797:1428–1438

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Acknowledgments

This work was supported by a scholarship (166340) from Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico.

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Authors and Affiliations

  1. Posgrado en Recursos Genéticos y Productividad-Fisiología Vegetal, Colegio de Postgraduados, Carretera México-Texcoco, km 36.5, Montecillo, 56230, México, México

    Huitziméngari Campos

  2. Posgrado en Botánica, Colegio de Postgraduados, Carretera México-Texcoco km 36.5, Montecillo, 56230, México, México

    Carlos Trejo, Cecilia B. Peña-Valdivia, Rodolfo García-Nava & F. Víctor Conde-Martínez

  3. Departamento de Ecología Funcional y Aplicada, Instituto de Ecología, Universidad Nacional Autónoma de México, Circuito Exterior, Ciudad Universitaria, 04510, México, D.F., México

    Ma. del Rocío Cruz-Ortega

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  1. Huitziméngari Campos
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  2. Carlos Trejo
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  3. Cecilia B. Peña-Valdivia
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Correspondence to Huitziméngari Campos.

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Campos, H., Trejo, C., Peña-Valdivia, C.B. et al. Photosynthetic acclimation to drought stress in Agave salmiana Otto ex Salm-Dyck seedlings is largely dependent on thermal dissipation and enhanced electron flux to photosystem I. Photosynth Res 122, 23–39 (2014). https://doi.org/10.1007/s11120-014-0008-6

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