Photosynthesis, Resource Acquisition and Growth Responses of Two Biomass Crops Subjected to Water Stress
Journal of Plant Sciences
Volume 6, Issue 3, June 2018, Pages: 68-86
Received: May 2, 2018; Accepted: May 19, 2018; Published: Jun. 25, 2018
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Authors
Elena Sánchez, Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Catalonia, Spain
Gladys Lino, Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Catalonia, Spain
Claudia Arias, Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Catalonia, Spain
Xavier Serrat, Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Catalonia, Spain
Salvador Nogués, Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Catalonia, Spain
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Abstract
This study compares photosynthesis, growth, 13C and 15N labelling patterns of two biomass crops (Arundo donax L. and Panicum virgatum L.) grown under water stress in greenhouse conditions. Plants were exposed to three water stress levels: control (C, 100% Pot Capacity), mild stress (MS, 50% PC) and severe stress (SS, 25% PC). Photosynthesis, fluorescence parameters and relative water content were measured at the beginning (Ti) and the end of the experiment (Tf). Biomass parameters were measured at Tf. Short-term double labelling with 13C and 15N stable isotopes was performed in both species. Isotopic analyses of total organic matter, total soluble sugars and the CO2 respired were undertaken at T0 (pre-labelling), T1 (24h after labelling) and T2 (7 days after labelling). Immediately after the 13C and 15N labelling, stems and rhizomes seemed to be the main sinks for labelled carbon and nitrogen in both species. Moreover, not all of the labelled carbon and nitrogen substrate was used by plant metabolism after seven days. Decreases in photosynthesis parameters were observed as a consequence of the increase in water stress (WS) in both species, with a greater magnitude decline in giant reed than in switchgrass. A decrease in height, number of green leaves and total dry weight due to WS was observed in both species. Both species were more 13C-enriched and more 15N-depleted during the increases in WS due to lower stomatal conductance and transpiration. In general, WS accelerated plant phenology and, consequently, the accumulation of storage compounds in the rhizome occurred in response to stress. This effect was more clearly visible in switchgrass than in giant reed.
Keywords
Arundo donax L., Panicum virgatum L., 13C and 15N Isotope Labelling, Biomass, Water Stress
To cite this article
Elena Sánchez, Gladys Lino, Claudia Arias, Xavier Serrat, Salvador Nogués, Photosynthesis, Resource Acquisition and Growth Responses of Two Biomass Crops Subjected to Water Stress, Journal of Plant Sciences. Vol. 6, No. 3, 2018, pp. 68-86. doi: 10.11648/j.jps.20180603.11
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Copyright © 2018 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
References
[1]
I. Lewandowski, J. M. O. Scurlock, E. Lindvall, M. Christou, The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe, Biomass and Bioenergy. 25 (2003) 335–361. doi:10.1016/S0961-9534(03)00030-8.
[2]
I. E. Palmer, R. J. Gehl, T. G. Ranney, D. Touchell, N. George, Biomass yield, nitrogen response, and nutrient uptake of perennial bioenergy grasses in North Carolina, Biomass and Bioenergy. 63 (2014) 218–228. doi:10.1016/J.biombioe.2014.02.016.
[3]
C. Mariani, R. Cabrini, A. Danin, P. Piffanelli, A. Fricano, S. Gomarasca, M. Dicandilo, F. Grassi, C. Soave, Origin, diffusion and reproduction of the giant reed (Arundo donax L.): a promising weedy energy crop, Ann. Appl. Biol. 157 (2010) 191–202. doi:10.1111/j.1744-7348.2010.00419.x.
[4]
L. G. Angelini, L. Ceccarini, N. N. o Di Nasso, E. Bonari, Comparison of Arundo donax L. and Miscanthus x giganteus in a long-term field experiment in Central Italy: Analysis of productive characteristics and energy balance, Biomass and Bioenergy. 33 (2009) 635–643. doi:https://doi.org/10.1016/j.biombioe.2008.10.005.
[5]
B. Rossa, A. V Tüffers, G. Naidoo, D. J. Willert, Arundo donax L. (Poaceae) — a C3 species with unusually high photosynthetic capacity, Bot. Acta. 111 (2014) 216–221. doi:10.1111/j.1438-8677.1998.tb00698.x.
[6]
J. N. Barney, J. J. Mann, G. B. Kyser, E. Blumwald, A. Van Deynze, J. M. DiTomaso, Tolerance of switchgrass to extreme soil moisture stress: Ecological implications, Plant Sci. 177 (2009) 724–732. doi:10.1016/j.plantsci.2009.09.003.
[7]
M. Gutierrez, V. E. Gracen, G. E. Edwards, Biochemical and cytological relationships in C4 plants, Planta. 119 (1974) 279–300. doi:10.1007/BF00388331.
[8]
M. D. Hatch, C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure, Biochim. Biophys. Acta - Rev. Bioenerg. 895 (1987) 81–106. doi:https://doi.org/10.1016/S0304-4173(87)80009-5.
[9]
C. L. Porter, An Analysis of Variation Between Upland and Lowland Switchgrass, Panicum Virgatum L., in Central Oklahoma, Ecology. 47 (1966) 980–992. doi:10.2307/1935646.
[10]
D. A. Warner, M. S. B. Ku, G. E. Edwards, Photosynthesis, leaf anatomy, and cellular constituents in the polyploid C4 Grass Panicum virgatum, Plant Physiol. 84 (1987) 461 LP-466. http://www.plantphysiol.org/content/84/2/461.abstract.
[11]
M. Sanderson, R. Reed, S. McLaughlin, S. Wullschleger, B. Conger, D. Parrish, D. Wolf, C. Taliaferro, A. Hopkins, W. Ocumpaugh, M. Hussey, J. Read, C. Tischler, Switchgrass as a sustainable crop, Bioresour. Technol. 56 (1996) 83–93.
[12]
M. D. Casler, C. M. Tobias, S. M. Kaeppler, C. R. Buell, Z.-Y. Wang, P. Cao, J. Schmutz, P. Ronald, The switchgrass genome: tools and strategies, 4 (2011). doi:10.3835/plantgenome2011.10.0026.
[13]
A. Yokota, K. Takahara, K. Akashi, Water stress, in: K. V Madhava Rao, A. S. Raghavendra, K. Janardhan Reddy (Eds.), Physiology and molecular bioliology of stress tolerance in plants, Springer Netherlands, Dordrecht, 2006: pp. 15–39. doi:10.1007/1-4020-4225-6_2.
[14]
H. Medrano, J. M. Escalona, J. Bota, J. Gulías, J. Flexas, Regulation of photosynthesis of C3plants in response to progressive drought: Stomatal conductance as a reference parameter, Ann. Bot. 89 (2002) 895–905. doi:10.1093/aob/mcf079.
[15]
J. Flexas, J. Bota, F. Loreto, G. Cornic, T. D. Sharkey, Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants, Plant Biol. 6 (2008) 269–279. doi:10.1055/s-2004-820867.
[16]
J. Flexas, A. Diaz-Espejo, J. Galmés, R. Kaldenhoff, H. Medrano, M. Ribas-Carbo, Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves, Plant, Cell Environ. 30 (2007) 1284–1298. doi:10.1111/j.1365-3040.2007.01700.x.
[17]
M. M. Chaves, J. Flexas, C. Pinheiro, Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell, Ann. Bot. 103 (2009) 551–560. doi:10.1093/aob/mcn125.
[18]
P. Kramer, J. Boyer, Cell water relations, in: Water Relations of Plants and Soils, 1st edn, 1995: pp. 42–83.
[19]
F. W. Badeck, G. Tcherkez, S. Nogues, C. Piel, J. Ghashghaie, Post-photosynthetic fractionation of stable carbon isotopes between plant organs - a widespread phenomenon, Rapid Commun Mass Spectrom. 19 (2005) 11. doi:10.1002/rcm.1912.
[20]
G. D. Farquhar, M. H. O’Leary, J. A. Berry, On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves, Funct. Plant Biol. 9 (1982) 121–137. https://doi.org/10.1071/PP9820121.
[21]
G. D. Farquhar, K. T. Hubick, A. G. Condon, R. A. Richards, Carbon isotope fractionation and plant water-use efficiency BT - Stable Isotopes in Ecological Research, in: P. W. Rundel, J. R. Ehleringer, K. A. Nagy (Eds.), Springer New York, New York, NY, 1989: pp. 21–40.
[22]
O. Ghannoum, S. von Caemmerer, J. P. Conroy, The effect of drought on plant water use efficiency of nine NAD-ME and nine NADP-ME Australian C4 grasses, Funct. Plant Biol. 29 (2002) 1337–1348. doi:http://dx.doi.org/10.1071/FP02056.
[23]
O. Ghannoum, C4 photosynthesis and water stress, Annu. Bot. 103 (2008) 635-644 doi:10.1093/aob/mcn093.
[24]
G. D. Farquhar, On the nature of carbon isotope discrimination in C4 species, Funct. Plant Biol. 10 (1983) 205–226. https://doi.org/10.1071/PP9830205.
[25]
J. Ghashghaie, F.W. Badeck, G. Lanigan, S. Nogués, G. Tcherkez, E. Deléens, G. Cornic, H. Griffiths, Carbon isotope fractionation during dark respiration and photorespiration in C3 plants, Phytochem. Rev. 2 (2003) 145–161. doi:10.1023/B:PHYT.0000004326.00711.ca.
[26]
E. A. Hobbie, R. A. Werner, Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis, New Phytol. 161 (2003) 371–385. doi:doi:10.1111/j.1469-8137.2004.00970.x.
[27]
L. A. Cernusak, N. Ubierna, K. Winter, J. A. M. Holtum, J. D. Marshall, G. D. Farquhar, Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants, New Phytol. 200 (2013) 950–965. doi:10.1111/nph.12423.
[28]
G. Tcherkez, M. Hodges, How stable isotopes may help to elucidate primary nitrogen metabolism and its interaction with (photo)respiration in C3 leaves, J. Exp. Bot. 59 (2008) 1685–1693. http://dx.doi.org/10.1093/jxb/erm115.
[29]
S. Nogués, N. R. Baker, Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation, J. Exp. Bot. 51 (2000) 1309–1317. http://dx.doi.org/10.1093/jxb/51.348.1309.
[30]
S. Nogués, S. Aljazairi, C. Arias, E. Sánchez, I. Aranjuelo, Two distinct plant respiratory physiotypes might exist which correspond to fast-growing and slow-growing species, J. Plant Physiol. 171 (2014) 1157–1163. doi:10.1016/J.JPLPH.2014.03.006.
[31]
S. Nogués, I. Aranjuelo, A. Pardo, J. Azcón-Bieto, Assessing the stable carbon isotopic composition of intercellular CO2 in a CAM plant using gas chromatography-combustion-isotope ratio mass spectrometry, Rapid Commun. Mass Spectrom. 22 (2008) 1017–1022. doi:10.1002/rcm.3460.
[32]
S. Nogués, G. Tcherkez, G. Cornic, J. Ghashghaie, Respiratory carbon metabolism following illumination in intact french bean leaves using 12C/13 isotope labeling, Plant Physiol. 136 (2004) 3245 LP-3254. http://www.plantphysiol.org/content/136/2/3245.abstract.
[33]
F. W. Badeck, G. Tcherkez, S. Nogués, C. Piel, J. Ghashghaie, Post-photosynthetic fractionation of stable carbon isotopes between plant organs—a widespread phenomenon, Rapid Commun. Mass Spectrom. 19 (2005) 1381–1391. doi:10.1002/rcm.1912.
[34]
J. D. Marshall, J. R. Brooks, K. Lajtha, Sources of variation in the stable isotopic composition of plants, Stable Isot. Ecol. Environ. Sci. 2 (2007) 22–60.
[35]
J. Ghashghaie, M. Duranceau, F. W. Badeck, G. Cornic, M. T. Adeline, E. Deleens, δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought, Plant. Cell Environ. 24 (2001) 505–515. doi:10.1046/j.1365-3040.2001.00699.x.
[36]
G. Tcherkez, S. Nogués, J. Bleton, G. Cornic, F. Badeck, J. Ghashghaie, Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in french bean, Plant Physiol. 131 (2003) 237 LP-244. http://www.plantphysiol.org/content/131/1/237.abstract.
[37]
M. Duranceau, J. Ghashghaie, F. Badeck, E. Deleens, G. Cornic, δ13C of CO2 respired in the dark in relation to δ13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought, Plant, Cell Environ. 22 (1999) 515–523. doi:10.1046/j.1365-3040.1999.00420.x.
[38]
A. A. Jaradat, Genetic resources of energy crops: Biological systems to combat climate change, AJCS. 4 (2010) 309–323. https://naldc.nal.usda.gov/naldc/download.xhtml?id=49241&content=PDF (accessed April 17, 2018).
[39]
T. L. Slewinski, Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production, J. Exp. Bot. 63 (2012) 4647–4670. http://dx.doi.org/10.1093/jxb/ers124.
[40]
S. Bihmidine, C. T. Hunter, C. E. Johns, K. E. Koch, D. M. Braun, Regulation of assimilate import into sink organs: update on molecular drivers of sink strength, Front. Plant Sci. 4 (2013) 177. doi:10.3389/fpls.2013.00177.
[41]
J. J. Mann, J. N. Barney, G. B. Kyser, J. M. Di Tomaso, Miscanthus × giganteus and Arundo donax shoot and rhizome tolerance of extreme moisture stress, GCB Bioenergy. 5 (2012) 693–700. doi:10.1111/gcbb.12039.
[42]
L. A. Cernusak, J. D. Marshall, J. P. Comstock, N. J. Balster, Carbon isotope discrimination in photosynthetic bark, Oecologia. 128 (2001) 24–35. http://www.jstor.org/stable/4222973.
[43]
J. Ghashghaie, F. W. Badeck, Opposite carbon isotope discrimination during dark respiration in leaves versus roots – a review, New Phytol. 201 (2014) 751–769. doi:10.1111/nph.12563.
[44]
R. F. Sage, R. W. Pearcy, The nitrogen use efficiency of C3 and C4 plants, Plant Physiol. 84 (1987) 959 LP-963. http://www.plantphysiol.org/content/84/3/959.abstract.
[45]
O. Ghannoum, J. R. Evans, S. von Caemmerer, Chapter 8 Nitrogen and water use efficiency of C4 plants BT - C4 Photosynthesis and related CO2 concentrating mechanisms, in: A. S. Raghavendra, R. F. Sage (Eds.), Springer Netherlands, Dordrecht, 2011: pp. 129–146. doi:10.1007/978-90-481-9407-0_8.
[46]
D. W. Lawlor, Limitation to photosynthesis in water‐stressed leaves: stomata vs. metabolism and the role of ATP, Ann. Bot. 89 (2002) 871–885.
[47]
J. Gulías, J. Flexas, A. Abadía, H. Madrano, Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species, Tree Physiol. 22 (2002) 687–697. http://dx.doi.org/10.1093/treephys/22.10.687.
[48]
D. Robinson, L. L. Handley, C. M. Scrimgeour, D. C. Gordon, B. P. Forster, R. P. Ellis, Using stable isotope natural abundances (δ15N and δ13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes, J. Exp. Bot. 51 (2000) 41–50. http://dx.doi.org/10.1093/jexbot/51.342.41.
[49]
S. Yousfi, M. D. Serret, J. Voltas, J. L. Araus, Effect of salinity and water stress during the reproductive stage on growth, ion concentrations, Δ13C, and δ15N of durum wheat and related amphiploids, J. Exp. Bot. 61 (2010) 3529–3542. http://dx.doi.org/10.1093/jxb/erq184.
[50]
R. J. Webster, S. M. Driever, J. Kromdijk, J. McGrath, A. D. B. Leakey, K. Siebke, T. Demetriades-Shah, S. Bonnage, T. Peloe, T. Lawson, S. P. Long, High C3 photosynthetic capacity and high intrinsic water use efficiency underlies the high productivity of the bioenergy grass Arundo donax, Sci. Rep. 6 (2016) 20694. http://dx.doi.org/10.1038/srep20694.
[51]
C. B. Osmond, K. Winter, H. Ziegler, Functional significance of different pathways of CO2 fixation in photosynthesis BT - Physiological Plant Ecology II: Water Relations and Carbon Assimilation, in: O. L. Lange, P. S. Nobel, C. B. Osmond, H. Ziegler (Eds.), Springer Berlin Heidelberg, Berlin, Heidelberg, 1982: pp. 479–547. doi:10.1007/978-3-642-68150-9_16.
[52]
L. L. Nackley, K. A. Vogt, S.-H. Kim, Arundo donax water use and photosynthetic responses to drought and elevated CO2, Agric. Water Manag. 136 (2014) 13–22. doi:10.1016/J.AGWAT.2014.01.004.
[53]
S. L. Cosentino, D. Scordia, E. Sanzone, G. Testa, V. Copani, Response of giant reed (Arundo donax L.) to nitrogen fertilization and soil water availability in semi-arid Mediterranean environment, Eur. J. Agron. 60 (2014) 22–32. doi:https://doi.org/10.1016/j.eja.2014.07.003.
[54]
E. Meyer, M. J. Aspinwall, D. B. Lowry, J. D. Palacio-Mejía, T. L. Logan, P. A. Fay, T. E. Juenger, Integrating transcriptional, metabolomic, and physiological responses to drought stress and recovery in switchgrass (Panicum virgatum L.), BMC Genomics. 15 (2014) 527.
[55]
G. Cornic, A. Massacci, Leaf photosynthesis under drought stress BT - Photosynthesis and the Environment, in: N. R. Baker (Ed.), Springer Netherlands, Dordrecht, 1996: pp. 347–366. doi:10.1007/0-306-48135-9_14.
[56]
J. M. Escalona, J. Flexas, H. Medrano, Stomatal and non-stomatal limitations of photosynthesis under water stress in field-grown grapevines, Aust. J. Plant Physiol. 26 (1999) 421. doi:10.1071/PP99019.
[57]
N. R. Baker, Chlorophyll Fluorescence: A probe of photosynthesis in vivo, Annu. Rev. Plant Biol. 59 (2008) 89–113. doi:10.1146/annurev.arplant.59.032607.092759.
[58]
T. D. Sharkey, Water-stress effects on photosynthesis, (1990).
[59]
F. Li, S. Kang, J. Zhang, Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat, Agric. Water Manag. 67 (2004) 221–233. doi:https://doi.org/10.1016/j.agwat.2004.01.005.
[60]
E. Heaton, T. Voigt, S. P. Long, A quantitative review comparing the yields of two candidate C4 perennial biomass crops in relation to nitrogen, temperature and water, Biomass and Bioenergy. 27 (2004) 21–30. doi:https://doi.org/10.1016/j.biombioe.2003.10.005.
[61]
M. Fagnano, A. Impagliazzo, M. Mori, N. Fiorentino, Agronomic and environmental impacts of Giant reed (Arundo donax L.): Results from a long-term field experiment in hilly areas subject to soil erosion, BioEnergy Res. 8 (2015) 415–422. doi:10.1007/s12155-014-9532-7.
[62]
A. Blum, Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive?, Aust. J. Agric. Res. 56 (2005) 1159–1168. doi:10.1071/AR05069.
[63]
G. Erice, S. Louahlia, J. J. Irigoyen, M. Sanchez-Diaz, J.-C. Avice, Biomass partitioning, morphology and water status of four alfalfa genotypes submitted to progressive drought and subsequent recovery, J. Plant Physiol. 167 (2010) 114–120. doi:https://doi.org/10.1016/j.jplph.2009.07.016.
[64]
P. J. Kramer, J. S. Boyer, Water relations of plants and soils, Academic press, 1995.
[65]
L. D. Quinn, K. C. Straker, J. Guo, S. Kim, S. Thapa, G. Kling, D. K. Lee, T. B. Voigt, Stress-tolerant feedstocks for sustainable bioenergy production on marginal land, Bioenergy Res. 8 (2015) 1081–1100. doi:10.1007/s12155-014-9557-y.
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