Photosynthetica 2020, 58(4):995-1008 | DOI: 10.32615/ps.2020.053

Implications of intra-seasonal climate variations on chlorophyll a fluorescence and biomass in winter barley breeding program

L. BEGOVIĆ1,†, V. GALIĆ2,†, I. ABIČIĆ2, Z. LONČARIĆ3, A. LALIĆ2, S. MLINARIĆ1
Department of Biology, Josip Juraj Strossmayer University of Osijek, Cara Hadrijana 8/A, HR-31000 Osijek, Croatia1
2 Agricultural Institute Osijek, Južno predgrađe 17, HR-31000 Osijek, Croatia
3 Faculty of Agrobiotechnical Sciences Osijek, Josip Juraj Strossmayer University of Osijek, Vladimira Preloga 1, HR-31000 Osijek, Croatia

This study aimed to explore how ten selected winter barley genotypes responded to variations in environmental conditions during the growth season by using fast chlorophyll a fluorescence and normalized difference vegetation index (NDVI) at the booting, anthesis and early grain-filling stage. Lower amount of rainfall during the anthesis induced instability in the function of PSII, observed as the positive K-band in six and the positive L-band in seven genotypes. At grain filling, all genotypes displayed negative K- and L-bands, suggesting an increase of stability within PSII. The performance index increased from booting to grain filling in most genotypes. Chlorophyll a fluorescence parameters were incorporated into the partial least squares model as explanatory variables of NDVI. After a cross-validation, the model with four latent variables was chosen explaining 75.8% variance (r = 0.870) for NDVI. The principal component analyses showed two distinct types of the reaction of the barley genotypes to the mild drought stress at anthesis.

Additional key words: abiotic stress; carbon; Hordeum vulgare L.; nitrogen.

Received: January 20, 2020; Revised: May 16, 2020; Accepted: July 7, 2020; Prepublished online: July 30, 2020; Published: September 4, 2020  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
BEGOVIĆ, L., GALIĆ, V., ABIČIĆ, I., LONČARIĆ, Z., LALIĆ, A., & MLINARIĆ, S. (2020). Implications of intra-seasonal climate variations on chlorophyll a fluorescence and biomass in winter barley breeding program. Photosynthetica58(4), 995-1008. doi: 10.32615/ps.2020.053
Download citation

Supplementary files

Download fileBegovic_2519_supplement.xlsx

File size: 296.29 kB

References

  1. Ahuja I., de Vos R.C.H., Bones A.M., Hall R.D.: Plant molecular stress responses face climate change. - Trends Plant Sci. 15: 664-674, 2010. Go to original source...
  2. Araus J.L., Cairns J.E.: Field high-throughput phenotyping: the new crop breeding frontier. - Trends Plant. Sci. 19: 52-61, 2014. Go to original source...
  3. Badr A., Müller K., Schäfer-Pregl R. et al.: On the origin and domestication history of barley (Hordeum vulgare). - Mol. Biol. Evol. 17: 499-510, 2000. Go to original source...
  4. Begović L., Mlinarić S., Antunović Dunić J. et al.: Response of Lemna minor L. to short-term cobalt exposure: The effect on photosynthetic electron transport chain and induction of oxidative damage. - Aquat. Toxicol. 175: 117-126, 2016. Go to original source...
  5. Brestič M., Živčák M., Hauptvogel P. et al.: Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. - Photosynth. Res. 136: 245-255, 2018. Go to original source...
  6. Bro R., Smilde A.K.: Principal component analysis. - Anal. Methods-UK 6: 2812-2831, 2014. Go to original source...
  7. Cabrera-Bosquet L., Molero G., Stellacci A. et al.: NDVI as a potential tool for predicting biomass, plant nitrogen content and growth in wheat genotypes subjected to different water and nitrogen conditions. - Cereal Res. Commun. 39: 147-159, 2011. Go to original source...
  8. Carillo P., Gibon Y.: Protocol: extraction and determination of proline, 2011. Available at: https://www.researchgate.net/publication/211353600_PROTOCOL_Extraction_and_determination_of_proline.
  9. Cassman K.G., Grassini P., van Wart J.: Crop yield potential, yield trends, and global food security in a changing climate. -In: Hillel D., Rosenzweig C. (ed.): Handbook of Climate Change and Agroecosystems: Impacts, Adaptation, and Mitigation. Pp. 37-51. World Scientific, Singapore 2011. Go to original source...
  10. Cavender-Bares J., Bazzaz F.A.: From leaves to ecosystems: using chlorophyll fluorescence to assess photosynthesis and plant function in ecological studies. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 737-755. Springer, Dordrecht 2004. Go to original source...
  11. Ceppi M.G., Oukarroum A., Çiçek N. et al.: 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. Plantarum 144: 277-288, 2012. Go to original source...
  12. Chen Y.-E., Liu W.-J., Su Y.-Q. et al.: Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. - Physiol. Plantarum 158: 225-235, 2016. Go to original source...
  13. Chen Y.-E., Yuan S., Du J.-B. et al.: Phosphorylation of photosynthetic antenna protein CP29 and photosystem II structure changes in monocotyledonous plants under environ-mental stresses. - Biochemistry 48: 9757-9763, 2009. Go to original source...
  14. Christen D., Schönmann S., Jermini M. et al.: Characterization and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. - Environ. Exp. Bot. 60: 504-514, 2007. Go to original source...
  15. Christopher J.T., Veyradier M., Borrell A.K. et al.: Phenotyping novel stay-green traits to capture genetic variation in senescence dynamics. - Funct. Plant. Biol. 41: 1035-1048, 2014. Go to original source...
  16. Daszkowska-Golec A., Collin A., Sitko K. et al.: Genetic and physiological dissection of photosynthesis in barley exposed to drought stress. - Int. J. Mol. Sci. 20: 6341, 2019. Go to original source...
  17. De Ronde J.A., Cress W.A., Krüger G.H.J. et al.: Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. - J. Plant Physiol. 161: 1211-1224, 2004. Go to original source...
  18. Din M., Zheng W., Rashid M. et al.: Evaluating hyperspectral vegetation indices for leaf area index estimation of Oryza sativa L. at diverse phenological stages. - Front. Plant Sci. 8: 820, 2017. Go to original source...
  19. Distelfeld A., Avni R., Fischer A.M.: Senescence, nutrient remobilization, and yield in wheat and barley. - J. Exp. Bot. 65: 3783-3798, 2014. Go to original source...
  20. Dordas C.: Variation in dry matter and nitrogen accumulation and remobilization in barley as affected by fertilization, cultivar, and source-sink relations. - Eur. J. Agron. 37: 31-42, 2012. Go to original source...
  21. Duan T., Chapman S., Guo Y., Zheng B.: Dynamic monitoring of NDVI in wheat agronomy and breeding trials using an unmanned aerial vehicle. - Field Crop. Res. 210: 71-80, 2017. Go to original source...
  22. Force L., Critchley C., van Rensen J.J.S.: New fluorescence parameters for monitoring photosynthesis in plants. - Photosynth. Res. 78: 17-33, 2003. Go to original source...
  23. Franić M., Jambrović A., Šimić D. et al.: Photosynthetic properties of maize hybrids under different environmental conditions probed by the chlorophyll a fluorescence. - Maydica 64: M25, 2020.
  24. Freeman K.W., Girma K., Arnall D.B. et al.: By-plant prediction of corn forage biomass and nitrogen uptake at various growth stages using remote sensing and plant height. - Agron. J. 99: 530-536, 2007. Go to original source...
  25. Galić V., Mazur M., Šimić D. et al.: Plant biomass in salt-stressed young maize plants can be modelled with photosynthetic performance. - Photosynthetica 57: 9-19, 2020. Go to original source...
  26. Gitelson A.A., Merzlyak M.N.: Remote estimation of chlorophyll content in higher plant leaves. - Int. J. Remote Sens. 18: 2691-2697, 1997. Go to original source...
  27. Goltsev V., Zaharieva I., Chernev P. et al.: 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, 2012. Go to original source...
  28. Gratani L., Catoni R., Varone L.: Morphological, anatomical and physiological leaf traits of Q. ilex, P. latifolia, P. lentiscus, and M. communis and their response to Mediterranean climate stress factors. - Bot. Stud. 54: 35, 2013. Go to original source...
  29. Hanjra M.A., Qureshi M.E.: Global water crisis and future food security in an era of climate change. - Food Policy 35: 365-377, 2010. Go to original source...
  30. Hansen P.M., Schjoerring J.K.: Reflectance measurement of canopy biomass and nitrogen status in wheat crops using normalized difference vegetation indices and partial least squares regression. - Remote Sens. Environ. 86: 542-553, 2003. Go to original source...
  31. Huang W., Yang Y.-J., Zhang S.-B., Liu T.: Cyclic electron flow around photosystem I promotes ATP synthesis possibly helping the rapid repair of photodamaged photosystem II at low light. - Front. Plant Sci. 9: 239, 2018. Go to original source...
  32. Humbeck K., Krupinska K.: The abundance of minor chlorophyll a/b binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light. - J. Exp. Bot. 54: 375-383, 2003. Go to original source...
  33. Jedmowski C., Ashoub A., Brüggemann W.: Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fluorescence transient analysis. - Acta Physiol. Plant. 35: 345-354, 2013. Go to original source...
  34. Jiang C.-D., Jiang G.-M., Wang X. et al.: Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP. - Environ. Exp. Bot. 58: 261-268, 2006. Go to original source...
  35. Kalaji H.M., Carpentier R., Allakhverdiev S.I., Bosa K.: Fluores-cence parameters as early indicators of light stress in barley. -J. Photoch. Photobio. B 112: 1-6, 2012. Go to original source...
  36. Kalaji H.M., Govindjee, Bosa K. et al.: Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. - Environ. Exp. Bot. 73: 64-72, 2011. Go to original source...
  37. Kalaji H.M., Guo P.: Chlorophyll fluorescence: a useful tool in barley plant breeding programs. - In: Sánchez A., Gutierrez S.J. (ed.): Photochemistry Research Progress. Pp. 439-463. Nova Science Publishers, Hauppauge 2008.
  38. Kalaji H.M., Jajoo A., Oukarroum A. et al.: Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant. 38: 102, 2016. Go to original source...
  39. Kalaji H.M., Rastogi A., Živčák M. et al.: Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. - Photosynthetica 56: 953-961, 2018. Go to original source...
  40. Kavi Kishor P.B., Hima Kumari P., Sunita M.S.L., Sreenivasulu N.: Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. - Front. Plant Sci. 6: 544, 2015. Go to original source...
  41. Krüger G.H.J., De Villiers M.F., Strauss A.J. et al.: Inhibition of photosystem II activities in soybean (Glycine max) genotypes differing in chilling sensitivity. - S. Afr. J. Bot. 95: 85-96, 2014. Go to original source...
  42. Kucharewicz W., Distelfeld A., Bilger W. et al.: Acceleration of leaf senescence is slowed down in transgenic barley plants deficient in the DNA/RNA-binding protein WHIRLY1. - J. Exp. Bot. 68: 983-996, 2017. Go to original source...
  43. Lalić A., Novoselović D., Kovačević J. et al.: Genetic gain and selection criteria effects on yield and yield components in barley (Hordeum vulgare L.). - Period. Biol. 112: 311-316, 2010.
  44. Lawlor D.W.: Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. - J. Exp. Bot. 53: 773-787, 2002. Go to original source...
  45. Lawlor D.W., Day W., Johnston A.E. et al.: Growth of spring barley under drought: crop development, photosynthesis, dry-matter accumulation and nutrient content. - J. Agr. Sci. 96: 167-186, 1981. Go to original source...
  46. Lehmann S., Funck D., Szabados L., Rentsch D.: Proline metabolism and transport in plant development. - Amino Acids 39: 949-962, 2010. Go to original source...
  47. Li F., Miao Y., Feng G. et al.: Improving estimation of summer maize nitrogen status with red edge-based spectral vegetation indices. - Field Crop. Res. 157: 111-123, 2014. Go to original source...
  48. Lichtenthaler H., Wenzel O., Buschmann C., Gitelson A.: Plant stress detection by reflectance and fluorescence. - Ann. N. Y. Acad. Sci. 851: 271-285, 1998. Go to original source...
  49. Liu X., Zhang H., Wang J. et al.: Increased CO2 concentrations increasing water use efficiency and improvement PSII function of mulberry seedling leaves under drought stress. - J. Plant Interact. 14: 213-223, 2019. Go to original source...
  50. Manojlović M.S., Lončarić Z., Cabilovski R.R. et al.: Bioforti-fication of wheat cultivars with selenium. - Acta Agr. Scand. B-S. P. 69: 715-724, 2019. Go to original source...
  51. Marinaccio F., Reyneri A., Blandino M.: Enhancing grain yield and quality of winter barley through agronomic strategies to prolong canopy greenness. - Field Crop. Res. 170: 109-118, 2015. Go to original source...
  52. Mevik B.-H., Wehrens R., Liland K.H.: pls: Partial least squares and principal component regression. R package version 2.7-0, 2018. Available at: https://CRAN.R-project.org/package=pls (Accessed 20 July 2020)
  53. Mlinarić S., Dunić J.A., Babojelić M.S. et al.: Differential accumulation of photosynthetic proteins regulates diurnal photochemical adjustments of PSII in common fig (Ficus carica L.) leaves. - J. Plant. Physiol. 209: 1-10, 2017. Go to original source...
  54. Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I.: Photoinhibition of photosystem II under environmental stress. - BBA-Bioenergetics 1767: 414-421, 2007. Go to original source...
  55. Oukarroum A., El Madidi S., Schansker G., Strasser R.J.: Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. - Environ. Exp. Bot. 60: 438-446, 2007. Go to original source...
  56. Oukarroum A., Schansker G., Strasser R.J.: 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. Plantarum 137: 188-199, 2009. Go to original source...
  57. Panda D., Sarkar R.K.: Natural leaf senescence: probed by chlorophyll fluorescence, CO2 photosynthetic rate and antioxidant enzyme activities during grain filling in different rice cultivars. - Physiol. Mol. Biol. Pla. 19: 43-51, 2013. Go to original source...
  58. Parrott D.L., McInnerney K., Feller U., Fischer A.M.: Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. - New Phytol. 176: 56-69, 2007. Go to original source...
  59. Parrott D.L., Yang L., Shama L., Fischer A.M.: Senescence is accelerated, and several proteases are induced by carbon "feast" conditions in barley (Hordeum vulgare L.) leaves. - Planta 222: 989-1000, 2005. Go to original source...
  60. Porter J.R., Semenov M.A.: Crop responses to climatic variation. -Philos. T. Roy. Soc. B 360: 2021-2035, 2005. Go to original source...
  61. Prasad P.V.V., Staggenborg S.A., Ristic Z.: Impacts of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. - In: Ahuja L.R., Reddy V.R., Saseendran S.A., Yu Q. (ed.): Response of Crops to Limited Water: Understanding and Modeling Water Stress Effects on Plant Growth Processes. Pp. 301-355. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison 2008. Go to original source...
  62. Rapacz M., Wójcik-Jagła M., Fiust A. et al.: Genome-wide associations of chlorophyll fluorescence OJIP transient parameters connected with soil drought response in barley. - Front. Plant Sci. 10: 78, 2019. Go to original source...
  63. Raun W.R., Solie J.B., Johnson G.V. et al.: In-season prediction of potential grain yield in winter wheat using canopy reflectance. - Agron. J. 93: 131-138, 2001. Go to original source...
  64. Redillas M.C.F.R., Strasser R.J., Jeong J.S. et al.: The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10. - Plant. Biotechnol. Rep. 5: 169-175, 2011. Go to original source...
  65. Reynolds M.P., Langridge P.: Physiological breeding. - Curr. Opin. Plant Biol. 31: 162-171, 2016. Go to original source...
  66. Reynolds M.P., Quilligan E., Aggarwal P.K. et al.: An integrated approach to maintaining cereal productivity under climate change. - Glob. Food Secur. 8: 9-18, 2016. Go to original source...
  67. Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluores-cence transient as a tool to characterize and screen photosyn-thetic samples. - In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445-483. Taylor & Francis, London 2000.
  68. Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V.: 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, 2010. Go to original source...
  69. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 321-362. Springer, Dordrecht 2004. Go to original source...
  70. Strauss A.J., Krüger G.H.J., Strasser R.J., Van Heerden P.D.R.: Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. - Environ. Exp. Bot. 56: 147-157, 2006. Go to original source...
  71. Sun Z.W., Ren L.K., Fan J.W. et al.: Salt response of photosynthetic electron transport system in wheat cultivars with contrasting tolerance. - Plant Soil Environ. 62: 515-521, 2016. Go to original source...
  72. Teulat B., Monneveux P., Wery J. et al.: Relationships between relative water content and growth parameters under water stress in barley: a QTL study. - New Phytol. 137: 99-107, 1997. Go to original source...
  73. Thomas H., Ougham H.: The stay-green trait. - J. Exp. Bot. 65: 3889-3900, 2014. Go to original source...
  74. Venkatesh J., Upadhyaya C.P., Yu J.-W. et al.: Chlorophyll a fluorescence transient analysis of transgenic potato over-expressing D-galacturonic acid reductase gene for salinity stress tolerance. - Hortic. Environ. Biote. 53: 320-328, 2012. Go to original source...
  75. Viljevac Vuletić M., Španić V.: Characterization of photo-synthetic performance during natural leaf senescence in winter wheat: Multivariate analysis as a tool for phenotypic characterization. - Photosynthetica 58: 301-313, 2020. Go to original source...
  76. Vu V.Q.: ggbiplot: A ggplot2 based biplot. R package version 0.55, 2011.
  77. Walsh O.S., Klatt A.R., Solie J.B. et al.: Use of soil moisture data for refined GreenSeeker sensor based nitrogen recommendations in winter wheat (Triticum aestivum L.). - Precis. Agric. 14: 343-356, 2013. Go to original source...
  78. Wold S., Esbensen K., Geladi P.: Principal component analysis. - Chemomet. Intell. Lab. Syst. 2: 37-52, 1987. Go to original source...
  79. Wu X., Tang Y., Li C. et al.: Chlorophyll fluorescence and yield responses of winter wheat to waterlogging at different growth stages. - Plant Prod. Sci. 18: 284-294, 2015. Go to original source...
  80. Xu X.-G., Yang X.-D., Gu X.-H. et al.: Monitoring the ratio of leaf carbon to nitrogen in winter wheat with hyperspectral measurements. Proc. SPIE 9637, Remote Sensing for Agriculture, Ecosystems, and Hydrology XVII, 96371N, 2015. doi.org/10.1117/12.2194937 Go to original source...
  81. Xu X., Yang G., Yang X. et al.: Monitoring ratio of carbon to nitrogen (C/N) in wheat and barley leaves by using spectral slope features with branch-and-bound algorithm. - Sci. Rep.-UK 8: 10034, 2018. Go to original source...
  82. Yusuf M.A., Kumar D., Rajwanshi R. et al.: 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, 2010. Go to original source...
  83. Zhang M., Shan Y., Kochian L. et al.: Photochemical properties in flag leaves of a super-high-yielding hybrid rice and a traditional hybrid rice (Oryza sativa L.) probed by chloro-phyll a fluorescence transient. - Photosynth. Res. 126: 275-284, 2015. Go to original source...
  84. Zhang Z., Li G., Gao H. et al.: Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence Zea mays L. inbred lines. - PLoS ONE 7: e42936, 2012. Go to original source...
  85. Żurek G., Rybka K., Pogrzeba M. et al.: Chlorophyll a fluorescence in evaluation of the effect of heavy metal soil contamination on perennial grasses. - PLoS ONE 9: e91475, 2014. Go to original source...
  86. Živčák M., Brestič M., Olšovská K., Slamka P.: Performance index as a sensitive indicator of water stress in Triticum aestivum L. - Plant Soil Environ. 54: 133-139, 2008. Go to original source...