Photosynthetica

, Volume 54, Issue 2, pp 275–287 | Cite as

Submergence-tolerant rice withstands complete submergence even in saline water: Probing through chlorophyll a fluorescence induction O-J-I-P transients

Original papers
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Abstract

Plants experience multiple abiotic stresses during the same growing season. The implications of submergence with and without saline water on growth and survival were investigated using four contrasting rice cultivars, FR13A (submergence-tolerant, salinity-susceptible), IR42 (susceptible to salinity and submergence), and Rashpanjor and AC39416 (salinity-tolerant, submergence-susceptible). Though both FR13A and IR42 showed sensitivity to salinity, FR13A exhibited higher initial biomass as well as maintained greater dry mass under saline condition. Greater reduction of chlorophyll (Chl) contents due to salinity was observed in the susceptible cultivars, including FR13A, compared to the salinity-tolerant cultivars. Exposure of plants to salinity before submergence decreased the survival chance under submergence. Yet, survival percentage under submergence was greater in FR13A compared to other cultivars. Generally, the reduction in the Chl content and damage to PSII were higher under the submergence compared to salinity conditions. The submergence-tolerant cultivar, FR13A, maintained greater quantities of Chl during submergence compared to other cultivars. Quantification of the Chl a fluorescence transients (JIP-test) revealed large cultivar differences in the response of PSII to submergence in saline and nonsaline water. The submergence-tolerant cultivar maintained greater chloroplast structural integrity and functional ability irrespective of the quality of flooding water.

Additional key words

energy flux Oryza sativa performance index saline flooding water stress tolerance 

Abbreviations

ABS/RC

quantum of light absorption per active reaction centre [M0 × (1/VJ) × (Fm/Fv)]

Chl

chlorophyll

C-SU-NW

normal growth, submergence with nonsaline water

C-SU-SW

normal growth, submergence with 12 dS m−1 saline water

ET0/ABS

electron transport per quantum of absorption of light [(Fv/Fm) × (1 − VJ)]

ET0/RC

electron transport per active reaction centre [M0 × (1/VJ) × (1 − VJ)]

F0

minimal fluorescence

Fm

maximal fluorescence

Fv

variable fluorescence (Fm − F0)

Fv/Fm

maximum photochemical efficiency of PSII

F50μs, F150μs, F300μs, and F2ms

fluorescence intensity at 50, 150, or 300 μs, and 2 ms, respectively

M0

initial slope of relative variable chlorophyll fluorescence [4 (F300μs − F50μs)/Fv]

OEC

oxygen evolving complex

PIABS

performance index on the basis of utilization of absorbed energy

RC/CS0

number of reaction centres per excited cross-section [Fv/Fm × (VJ/M0) × F0]

S-SU-NW

12 dS m−1 saline treatment before submergence, submergence with nonsaline water

S-SU-SW

12 dS m−1 saline treatment before submergence, submergence with 12 dS m−1 saline water

TR0/RC

quantum of light utilized per reaction centre [M0 × (1/VJ)]

VI

relative variable fluorescence at time 30 ms (I-step) after start of actinic light pulse [(F30ms − F50μs)/(Fm − F50μs)]

VJ

relative variable fluorescence at time 2 ms (J-step) after start of actinic light pulse [(F2ms − F0)/(Fm − F0)]

ΔVI–P

amplitude of the IP-phase [(1 − VI) = (Fm − F30ms)/(Fm − F50μs)]

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References

  1. Aro E.-M., Virgin I., Andersson B.: Photo-inhibition of photosystem II. Inactivation, protein damage and turnover. — Biochim. Biophys. Acta 1143: 113–134, 1993.CrossRefPubMedGoogle Scholar
  2. Bennett S.J., Barrett-Lennard E.G., Colmer T.D.: Salinity and waterlogging as constraints to saltland pasture production: A review. — Agr. Ecosyst. Environ. 129: 349–360, 2009.CrossRefGoogle Scholar
  3. Björkman, O., Demmig B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins. — Planta 170: 489–504, 1987.CrossRefPubMedGoogle Scholar
  4. Breštic M., Živcák M., Kalaji H.M. et al.: Photosystem II thermostability in situ: Environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. — Plant Physiol. Biochem. 57: 93–105, 2012.CrossRefPubMedGoogle Scholar
  5. Das K.K., Panda D., Sarkar R.K. et al.: Submergence tolerance in relation to variable floodwater conditions in rice. — Environ. Exp. Bot. 66: 425–434, 2009.CrossRefGoogle Scholar
  6. Das K.K., Sarkar R.K., Ismail A.M.: Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice. — Plant Sci. 168: 131–136, 2005.CrossRefGoogle Scholar
  7. Demmig-Adams B., Adams III W.W.: Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. — New Phytol. 172: 11–21, 2006.CrossRefPubMedGoogle Scholar
  8. Desotgiu R., Pollastrini M., Cascio C. et al.: Chlorophyll a fluorescence analysis along a vertical gradient of the crown in a poplar (Oxford clone) subjected to ozone and water stress. — Tree Physiol. 32: 976–986, 2012.CrossRefPubMedGoogle Scholar
  9. Douglas I.: Climate change, flooding and food security in south Asia. — Food Secur. 1: 127–136, 2009.CrossRefGoogle Scholar
  10. Duarte B., Santos D., Marques J.C. et al.: Biophysical probing of Spartina maritima photo-system II changes during prolonged tidal submersion periods. — Plant Physiol. Bioch. 77: 122–132, 2014.CrossRefGoogle Scholar
  11. Fini A., Bellasio C., Pollastri S. et al.: Water relations, growth, and leaf gas exchange as affected by water stress in Jatropha curcas. — J. Arid Environ. 89: 21–29, 2013.CrossRefGoogle Scholar
  12. Gorai M., Ennajeh M., Khemira H. et al.: Combined effect of NaCl-salinity and hypoxia on growth, photosynthesis, water relations and solute accumulation in Phragmites australis plants. — Flora 205: 462–470, 2010.CrossRefGoogle Scholar
  13. Chang T.T.: Rice. — In: Kiple K.F., Ornelas K.C. (ed.): The Cambridge World History of Food, Chapter II. A. 7. Pp. 132–149. Cambridge University Press, Cambridge 2000.Google Scholar
  14. Chen Y., Zhou Y., Yin T-F. et al.: The invasive wetland plant Alternanthera philoxeroides shows a higher tolerance to waterlogging than its native congener Alternanthera sessilis. — PLoS ONE 8: e81456, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Jiang C.D., Shi L., Gao H.Y. et al.: Development of photosystem 2 and 1 during leaf growth in grapevine seedlings probed by chlorophyll a fluorescence transient and 820 nm transmission in vivo. — Photosynthetica 44: 454–463, 2006.CrossRefGoogle Scholar
  16. Kalaji M.H., Bosa K., Koscielniak J. et al.: Chlorophyll a fluorescence — a useful tool for the early detection of temperature stress in spring barley (Hordeum vulgare L.). — OMICS 15: 925–934, 2011.CrossRefPubMedGoogle Scholar
  17. Kalaji M.H., Carpentier R., Allakhverdiev S.I. et al.: Fluorescence parameters as an early indicator of light stress in barley. — J. Photoch. Photobio. B 112: 1–6, 2012.CrossRefGoogle Scholar
  18. Kalaji M.H., Pietkiewicz S.: Salinity effects on plant growth and other physiological processes. — Acta Physiol. Plant. 15: 89–124, 1993.Google Scholar
  19. Kalaji M.H., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. — Photosynth. Res. 122: 121–158, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lazár D., Schansker G.: Models of chlorophyll a fluorescence transients. — In: Laisk A., Nedbal L., Govindjee (ed.): Photosynthesis in Silico: Understanding Complexity from Molecules to Ecosystems. Vol. 29. Pp. 85–123. Springer, Dordrecht 2009.CrossRefGoogle Scholar
  21. Lazár D.: Chlorophyll a fluorescence induction. — BBA-Bioenergetics 1412: 1–28, 1999.CrossRefPubMedGoogle Scholar
  22. Lazár D.: Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. — J. Theor. Biol. 220: 469–503, 2003.CrossRefPubMedGoogle Scholar
  23. Lazár D.: The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. — Func. Plant Biol. 33: 9–30, 2006.CrossRefGoogle Scholar
  24. Lazár D.: Parameters of photosynthetic energy partitioning. — J. Plant Physiol. 175: 131–147, 2015.CrossRefPubMedGoogle Scholar
  25. Lee S.-E., Yoo S.Y., Kim D.-Y. et al.: Proteomic evaluation of the response of soybean (Glycine max var. Seoritae) leaves to UV-B. — Plant Omics J. 7: 123–132, 2014.Google Scholar
  26. Long S.P., Humphries S., Falkowski P.G.: Photoinhibition of photosynthesis in nature. — Annu. Rev. Plant Phys. 45: 633–662, 1994.CrossRefGoogle Scholar
  27. Luo F-L., Chen Y., Huang L. et al.: Shifting effects of physiological integration on performance of a clonal plant during submergence and de-submergence. — Ann. Bot.-London 113: 1265–1274, 2014.CrossRefGoogle Scholar
  28. Mahata K.R., Singh D.P., Saha S. et al.: Improving rice productivity in the coastal saline soils of the Mahanadi Delta of India through integrated nutrient management. — In: Hoanh T.C., Szuster B.W., Suan-Peng K. et al. (ed.): Tropical Deltas and Coastal Zones: Food Production, Communities and Environment at the Land-Water Interface. Vol. 9. Pp. 239–248. CABI, Oxfordshire 2010.CrossRefGoogle Scholar
  29. Murchie E.H., Lawson T.: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. — J. Exp. Bot. 64: 3983–3998, 2013.CrossRefPubMedGoogle Scholar
  30. Oukarroum A., Bussotti F., Goltsev V. et al.: Correlation between reactive oxygen species production and photochemistry of photosyntem I and II in Lemna gibba L. plants under salt stress. — Environ. Exp. Bot. 109: 80–88, 2014.CrossRefGoogle Scholar
  31. Oukarroum A., Madidi S.E., Schansker G. et al.: 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, 2007.CrossRefGoogle Scholar
  32. Panda D., Rao D. N., Sharma S.G. et al.: Submergence effects on rice genotypes during seedling stage: Probing of submergence driven changes of photosystem 2 by chlorophyll a fluorescence induction O-J-I-P transients. — Photosynthetica 44: 69–75, 2006.CrossRefGoogle Scholar
  33. Panda D., Sarkar R. K.: Role of non-structural carbohydrate and its catabolism associated with SUB1 QTL in rice subjected to complete submergence. — Exp. Agric. 48: 502–512, 2012.CrossRefGoogle Scholar
  34. Panda D., Sharma S. G., Sarkar R. K.: Fast chlorophyll fluorescence transients as selection tools for submergence tolerance in rice (Oryza sativa). — Indian J. Agric. Sci. 78: 933–938, 2008a.Google Scholar
  35. Panda D., Sharma S.G., Sarkar R.K.: Chlorophyll fluorescence parameters, CO2 photosynthetic rate and regeneration capacity as a result of complete submergence and subsequent re-emergence in rice (Oryza sativa L.). — Aquat. Bot. 88: 127–133, 2008b.CrossRefGoogle Scholar
  36. Perboni A.T., Cassol D., Paulino da Silva F.S.P. et al.: Chlorophyll a fluorescence study revealing effects of flooding in canola hybrids. — Biologia 67: 338–346, 2012.CrossRefGoogle Scholar
  37. Porra R.J.: The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. — Photosynth. Res. 73: 149–156, 2002.CrossRefPubMedGoogle Scholar
  38. Qin X., Li F., Chen X., Xie Y.: Growth responses and nonstructural carbohydrates in three wetland macrophyte species following submergence and de-submergence. — Acta Physiol. Plant. 35: 2069–2074, 2013.CrossRefGoogle Scholar
  39. Rogers M.E., Colmer T.D., Nichols P.G.H. et al.: Salinity and waterlogging tolerance amongst accessions of messina (Melilotus siculus). — Crop Pasture Sci. 62: 225–235, 2011.CrossRefGoogle Scholar
  40. Salvatori E., Fusaro L., Mereu S. et al.: Different O3 response of sensitive and resistant snap bean genotypes (Phaseolus vulgaris L.): The key role of growth stage, stomatal conductance, and PSI activity. — Environ. Exp. Bot. 87: 79–91, 2013.CrossRefGoogle Scholar
  41. Sarkar R.K., Bhattacharjee B.: Rice genotypes with Sub1 QTL differ in submergence tolerance, elongation ability during submergence, and re-generation growth at re-emergence. — Rice 5: 7, 2011.Google Scholar
  42. Sarkar R.K., Mahata K.R., Singh D.P.: Differential responses of antioxidant system and photosynthetic characteristics in four rice cultivars differing in sensitivity to sodium chloride stress. — Acta Physiol. Plant. 35: 2915–2926, 2013.CrossRefGoogle Scholar
  43. Sarkar R.K., Panda D.: Distinction and characterisation of submergence tolerant and sensitive rice cultivars, probed by the fluorescence OJIP rise kinetics. — Func. Plant Biol. 36: 222–233, 2009.CrossRefGoogle Scholar
  44. Sarwar G.M., Khan M.H.: Sea level rise: A threat to the coast of Bangladesh. — Intl. Asienforum 38: 375–397, 2007.Google Scholar
  45. Singh D.P., Sarkar R.K.: Distinction and characterization of salinity tolerant and sensitive rice cultivars as probed by the chlorophyll fluorescence characteristics and growth parameters. — Func. Plant Biol. 41: 727–736, 2014.CrossRefGoogle Scholar
  46. Singh D.P., Mahata K.R., Saha S. et. al.: Crop diversification for improving water productivity and rural livelihoods in coastal saline soils of the Mahanadi delta, India. ? In: Hoanh C.T., Szuster B.W., Suan-peng K. et al. (ed.): Tropical Deltas and coastal Zones: Food Production, Communities and Environment at the Land-Water Interface. Vol. 9. Pp. 249–263. CABI, Oxfordshire, UK 2010.CrossRefGoogle Scholar
  47. Song J., Shi G.W., Gao B. et al.: Waterlogging and salinity effects on two Suaeda salsa populations. — Physiol. Plantarum 41: 343–351, 2011.CrossRefGoogle Scholar
  48. Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. — J. Photoch. Photobio. B 104: 236–257, 2011.CrossRefGoogle Scholar
  49. Strasser A., Tsimilli-Michael M., Srivastava A.: Analysis of the fluorescence transient. — In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration Series. Pp. 321–362. Springer, Dordrecht 2004.CrossRefGoogle Scholar
  50. Strasser B.J., Strasser R.J.: Measuring fast fluorescence transients to address environmental questions: The JIP-test. — In: Mathis P. (ed.): Photosynthesis: From Light to Biosphere. Vol. V. Pp. 977–980. Kluwer Academic Publ., London 1995.Google Scholar
  51. Strasser R.J., Govindjee: On the O-J-I-P fluorescence transients in leaves and D1 mutants of Chlamydomonas reinhardtii. — In: Murata N. (ed.): Research in Photosynthesis. Vol 11. Pp. 29–32. Kluwer Academic, Dordrecht 1992.Google Scholar
  52. Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples. — In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445–483. Tayor and Francis, New York 2000.Google Scholar
  53. Strasser R.J., Stirbet A.D.: Heterogeneity of Photosystem II probed by the numerically simulated chlorophyll a fluorescence rise (O-J-I-P). — Math. Comput. Simulat. 48: 3–9, 1998.CrossRefGoogle Scholar
  54. Teakle N.L., Colmer T.D., Pedersen O.: Leaf gas films delay salt entry and enhance underwater photosynthesis and internal aeration of Melilotus siculus submerged in saline water. — Plant Cell Environ. 37: 2339–2349, 2014.PubMedGoogle Scholar
  55. Wassmann R., Jagadish S.V.K., Heuer S. et al.: Climate change affecting rice production: The physiological and agronomic basis for possible adaptation strategies. — Adv. Agron. 101: 60–122, 2009.Google Scholar
  56. Winkel A., Pedersen O., Ella E. et al.: Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. — J. Exp. Bot. 65: 3225–3233, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  57. World Bank: Climate Change Impacts in Drought and Flood Affected Areas: Case Studies in India. Report No. 43946-IN. Pp. 1–162. The World Bank, Washington DC 2008.Google Scholar
  58. Xing D., Wu Y.: Effect of phosphorus deficiency on photosynthetic inorganic carbon assimilation of three climber plant species. — Bot. Stud. 55: 60–67, 2014.CrossRefGoogle Scholar
  59. Yan K., Shao H., Shao C. et al.: Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. — Acta Physiol. Plant. 35: 2867–2878, 2013.CrossRefGoogle Scholar
  60. Yoshida S., Forno D., Cock J. et al.: Determination of sugar and starch in plant tissue. — In: Laboratory Manual for Physiological Studies of Rice. Pp. 46–49. International Rice Research Institute, Los Ban?s 1976.Google Scholar
  61. Živcák M., Breštic M., Kalaji H. M. et al.: Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? — Photosynth. Res. 119: 339–354, 2014.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2016

Authors and Affiliations

  1. 1.Division of Crop Physiology and BiochemistryICAR-Central Rice Research InstituteCuttackIndia

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