Abstract
Water use efficiency (WUE) is an important physiological trait that has potential in sustaining crop productivity under water-limited condition. WUE can be increased by improving carbon gain and/or reducing transpiration. Normally, carbon gain and transpiration are inter-related and hence a trade-off exists between transpiration and WUE. Therefore, factors that influence these traits and their inter-relationship need to be identified and characterised. Here we report that leaf mass area (LMA) has one such trait that regulate WUE by influencing carbon gain. Extensive screening of EMS induced mutant population of Nagina-22 (N22) led to identification of contrasting LMA mutants. The high LMA mutant with 27% higher LMA (5.10 mg cm−2) than N22, and a low LMA mutant (4.00 mg cm−2) with comparable canopy leaf area and root weight were selected to study the influence of stomatal density and size on cumulative water transpired (CWT) and WUE under two soil moisture conditions (100% FC and 50% FC). The high LMA mutant, had higher stomatal density leading to increased CWT. But, a reduction in stomatal size on both abaxial and adaxial surfaces under water-limited conditions did not influence CWT. Increased photosynthetic efficiency due to higher leaf thickness led to higher carbon gain and hence higher WUE. The results indicate that improving carbon assimilation through higher LMA would significantly circumvent the trade-off between water loss and biomass accumulation leading to higher WUE. Thus, high chloroplast capacity types would have higher WUE despite relatively high water use.
Similar content being viewed by others
References
Aharoni, A., Dixit, S., Jetter, R., Thoenes, E., Van Arkel, G., & Pereira, A. (2004). The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. The Plant Cell, 16(9), 2463–2480.
Arredondo, J. T., & Schnyder, H. (2003). Components of leaf elongation rate and their relationship to specific leaf area in contrasting grasses. New Phytologist, 158(2), 305–314.
Bertolino, L. T., Caine, R. S., & Gray, J. E. (2019). Impact of stomatal density and morphology on water-use efficiency in a changing world. Frontiers in Plant Science, 10, 225.
Blake, T. J., Tschaplinski, T. J., & Eastham, A. (1984). Stomatal control of water use efficiency in poplar clones and hybrids. Canadian Journal of Botany, 62(7), 1344–1351.
Blum, A. (2011). Drought resistance—Is it really a complex trait? Functional Plant Biology, 38(10), 753–757.
Caine, R. S., Yin, X., Sloan, J., Harrison, E. L., Mohammed, U., Fulton, T., et al. (2019). Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytologist, 221(1), 371–384.
Condon, A. G., Richards, R. A., Rebetzke, G. J., & Farquhar, G. D. (2004). Breeding for high water-use efficiency. Journal of Experimental Botany, 55(407), 2447–2460.
Elliott, J., Deryng, D., Müller, C., Frieler, K., Konzmann, M., Gerten, D., et al. (2014). Constraints and potentials of future irrigation water availability on agricultural production under climate change. Proceedings of the National Academy of Sciences, 111(9), 3239–3244.
Evans, J., & Poorter, H. (2001). Photosynthetic acclimation of plants to growth irradiance: The relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell and Environment, 24(8), 755–767.
Fageria, N. K. (2003). Plant tissue test for determination of optimum concentration and uptake of nitrogen at different growth stages in lowland rice. Communications in Soil Science and Plant Analysis, 34(1–2), 259–270.
Fageria, N. K. (2007). Yield physiology of rice. Journal of Plant Nutrition, 30(6), 843–879.
Farooq, M., Hussain, M., Ul-Allah, S., & Siddique, K. H. (2019). Physiological and agronomic approaches for improving water-use efficiency in crop plants. Agricultural Water Management, 219, 95–108.
Farooq, M., Hussain, M., Wahid, A., & Siddique, K. H. M. (2012). Drought stress in plants: An overview. In Plant responses to drought stress (pp. 1–33). Berlin: Springer.
Franks, P. J., Doheny-Adams, T. W., Britton-Harper, Z. J., & Gray, J. E. (2015). Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytologist, 207(1), 188–195.
Garg, A. K., Kim, J. K., Owens, T. G., Ranwala, A. P., Do Choi, Y., Kochian, L. V., et al. (2002). Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences, 99(25), 15898–15903.
Harrison, E. L., Arce Cubas, L., Gray, J. E., & Hepworth, C. (2020). The influence of stomatal morphology and distribution on photosynthetic gas exchange. The Plant Journal, 101(4), 768–779.
Hughes, J., Hepworth, C., Dutton, C., Dunn, J. A., Hunt, L., Stephens, J., et al. (2017). Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiology, 174(2), 776–787.
Jarvis, P. G., & McNaughton, K. G. (1986). Stomatal control of transpiration: Scaling up from leaf to region. In Advances in ecological research (vol. 15, pp. 1–49). Academic Press.
Korres, N. E., Norsworthy, J. K., Burgos, N. R., & Oosterhuis, D. M. (2017). Temperature and drought impacts on rice production: An agronomic perspective regarding short-and long-term adaptation measures. Water Resources and Rural Development, 9, 12–27.
Mithra, S. A., Kar, M. K., Mohapatra, T., Robin, S., Sarla, N., Sheshashayee, M., et al. (2016). DBT propelled national effort in creating mutant resource for functional genomics in rice. Current Science, 110, 543–548.
Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science, 11, 15–19.
Mohapatra, T., Robin, S., Sarla, N., Sheshashayee, M., Singh, A. K., Singh, K., et al. (2014). EMS induced mutants of upland rice variety Nagina22: Generation and characterization. Proceedings of the Indian National Science Academy, 80(1), 163–172.
Moreno, E. A., McKown, A. D., Guy, R. D., & Soolanayakanahally, R. Y. (2016). Leaf mass per area predicts palisade structural properties linked to mesophyll conductance in balsam poplar (Populus balsamifera L.). Botany, 94(3), 225–239.
Morison, J. I. (1985). Sensitivity of stomata and water use efficiency to high CO2. Plant, Cell and Environment, 8(6), 467–474.
Nguyen, H. T., Babu, R. C., & Blum, A. (1997). Breeding for drought resistance in rice: Physiology and molecular genetics considerations. Crop Science, 37(5), 1426–1434.
Perdomo, J. A., Capó-Bauçà, S., Carmo-Silva, E., & Galmés, J. (2017). Rubisco and rubisco activase play an important role in the biochemical limitations of photosynthesis in rice, wheat, and maize under high temperature and water deficit. Frontiers in Plant Science, 8, 490.
Poorter, H., Niinemets, Ü., Poorter, L., Wright, I. J., & Villar, R. (2009). Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis. New Phytologist, 182(3), 565–588.
Praba, M. L., Cairns, J. E., Babu, R. C., & Lafitte, H. R. (2009). Identification of physiological traits underlying cultivar differences in drought tolerance in rice and wheat. Journal of Agronomy and Crop Science, 195(1), 30–46.
Raju, B. R., Narayanaswamy, B. R., Mohankumar, M. V., Sumanth, K. K., Rajanna, M. P., Mohanraju, B., et al. (2014). Root traits and cellular level tolerance hold the key in maintaining higher spikelet fertility of rice under water limited conditions. Functional Plant Biology, 41, 930–939.
Rang, Z. W., Jagadish, S. V. K., Zhou, Q. M., Craufurd, P. Q., & Heuer, H. (2011). Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environmental and Experimental Botany, 70, 58–65.
Reddy, S. H., Kambalimath, S. K., Singhal, R. K., Chikkakariyappa, M. K., Muthurajan, R., Rajanna, M. P., et al. (2019). Allele-specific analysis of single parent backcross population identifies HOX10 transcription factor as a candidate gene regulating rice root growth. Physiologia Plantarum, 166(2), 596–611.
Reddy, S. H., Singhal, R. K., DaCosta, M. V. J., Kambalimath, S. K., Rajanna, M. P., Muthurajan, R., et al. (2020). Leaf mass area determines water use efficiency through its influence on carbon gain in rice mutants. Physiologia Plantarum, 169(2), 194–213.
Richards, R. A. (2000). Selectable traits to increase crop photosynthesis and yield of grain crops. Journal of Experimental Botany, 51, 447–458.
Ritchie, J. T. (1972). Model for predicting evaporation from a row crop with incomplete cover. Water Resources Research, 8(5), 1204–1213.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676–682.
Sheshshayee, M. S., Bindumadhava, H., Shankar, A. G., Prasad, T. G., & Udayakumar, M. (2003). Breeding strategies to exploit water use efficiency for crop improvement. Journal of Plant Biology, 30(2), 253–268.
Sheshshayee, M. S., Vijayaraghavareddy, P., Sreevathsa, R., Rajendrareddy, S., Arakesh, S., Bharti, P., et al. (2018). Introgression of physiological traits for a comprehensive improvement of drought adaptation in crop plants. Frontiers in Chemistry, 6, 92.
Takai, T., Kondo, M., Yano, M., & Yamamoto, T. (2010). A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice. Rice, 3(2–3), 172–180.
Tanguilig, V. C., Yambao, E. B., O’toole, J. C., & De Datta, S. K. (1987). Water stress effects on leaf elongation, leaf water potential, transpiration, and nutrient uptake of rice, maize, and soybean. Plant and Soil, 103(2), 155–168.
Terashima, I., Hanba, Y. T., Tholen, D., & Niinemets, Ü. (2011). Leaf functional anatomy in relation to photosynthesis. Plant Physiology, 155(1), 108–116.
Vijayaraghavareddy, P., Xinyou, Y. I. N., Struik, P. C., Makarla, U., & Sreeman, S. (2020). Responses of lowland, upland and aerobic rice genotypes to water limitation during different phases. Rice Science, 27(4), 345–354.
Wang, H., Sánchez-Molina, J. A., Li, M., Berenguel, M., Yang, X. T., & Bienvenido, J. F. (2017). Leaf area index estimation for a greenhouse transpiration model using external climate conditions based on genetics algorithms, back-propagation neural networks and nonlinear autoregressive exogenous models. Agricultural Water Management, 183, 107–115.
Witkowski, E. T. F., & Lamont, B. B. (1991). Leaf specific mass confounds leaf density and thickness. Oecologia, 88(4), 486–493.
Xiong, X. D., Wang, D., Liu, X., Peng, S., Huang, J., & Li, Y. (2016). Leaf density explains variation in leaf mass per area in rice between cultivars and nitrogen treatments. Annals of Botany, 117(6), 963–971.
Acknowledgements
This research work was financially supported by Department of Biotechnology, New Delhi (Project No. BT/PR10787/AGIII/103/883/2014). Authors thank Prof. Udayakumar M and Prof T.G. Prasad for technical discussions and critical suggestions during the conduct of experiments. Authors also thank Dr. MS. Bobji, Assistant professor, Department of Mechanical Engineering, Indian Institute of Science, for use of scanning electron microscope facility of the department. Dr. Trilochan Mohapatra, Director General, ICAR and Secretary DARE government of India, was instrumental in initiating this program on development and characterization of rice mutants in India.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Reddy, S.H., Da Costa, M.V.J., Kambalimath, S.K. et al. Relative contribution of stomatal parameters in influencing WUE among rice mutants differing in leaf mass area. Plant Physiol. Rep. 25, 483–495 (2020). https://doi.org/10.1007/s40502-020-00537-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40502-020-00537-1