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Root anatomical traits of wild-rices reveal links between flooded rice and dryland sorghum

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Abstract

The root anatomical and morphological traits and their plasticity under water deficit are essential to improve adaptation of rice cultivars to water-limited conditions. We investigated wild-rice accessions along with a dryland cereal (Sorghum bicolor) for root related traits under non-stress and water deficit during panicle initiation and flowering. Wild-rices from GG genome (Oryza granulata and Oryza meyeriana) recorded high similarity with sorghum in key root anatomical parameters such as larger stele diameter in proportion to root diameter (SD:RD [%]) and more late metaxylem number (LMXN). Comparative analyses between wild-rice accessions and a diverse indica panel revealed narrow genetic variability in LMXN and SD:RD in Oryza sativa panel compared to O. granulata and O. meyeriana. Wild-rices from GG genome had a combination of favorable anatomy (larger SD:RD and more but smaller late metaxylem) and root morphology (thinner roots and higher root surface area) during panicle initiation and flowering compared to popular rice cultivar IR64. The above combination can help facilitate effective water use by regulating axial water flow under water-deficit conditions, while the opposite was noticed in the drought susceptible IR64. Novel sources for root anatomical traits identified from wild-rice accessions can be utilized in rice breeding programs to develop water-deficit stress tolerant rice cultivars.

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References

  • Abràmoff, M. D., Magalhães, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–43.

    Google Scholar 

  • Atwell, B. J., Wang, H., & Scafaro, A. P. (2014). Could abiotic stress tolerance in wild relatives of rice be used to improve Oryza sativa? Plant Science, 215, 48–58.

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen, J. L., & Freeling, M. (1993). Grasses as a single genetic system: Genome composition, collinearity and compatibility. Trends in Genetics, 9, 259–261.

    Article  CAS  PubMed  Google Scholar 

  • Bouman, B. A. M., Peng, S., Castaneda, A. R., & Visperas, R. M. (2005). Yield and water use of irrigated tropical aerobic rice systems. Agricultural Water Management, 74, 87–105.

    Article  Google Scholar 

  • Chimungu, J. G., Brown, K. M., & Lynch, J. P. (2014a). Reduced root cortical cell file number improves drought tolerance in maize. Plant Physiology, 166, 1943–1955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chimungu, J. G., Brown, K. M., & Lynch, J. P. (2014b). Large root cortical cell size improves drought tolerance in maize. Plant Physiology, 166, 2166–2178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chimungu, J. G., Loades, K. W., & Lynch, J. P. (2015a). Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea mays). Journal of Experimental Botany, 66, 3151–3162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chimungu, J. G., Maliro, M. F., Nalivata, P. C., Kanyama-Phiri, G., Brown, K. M., & Lynch, J. P. (2015b). Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.). Field Crops Research, 171, 86–98.

    Article  Google Scholar 

  • Christin, P. A., Osborne, C. P., Chatelet, D. S., Columbus, J. T., Besnard, G., Hodkinson, T. R., et al. (2013). Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proceedings of the National Academy of Sciences, 110, 1381–1386.

    Article  Google Scholar 

  • Comas, L., Becker, S., Cruz, V. M. V., Byrne, P. F., & Dierig, D. A. (2013). Root traits contributing to plant productivity under drought. Frontiers in plant science, 4, 442.

    Article  PubMed  PubMed Central  Google Scholar 

  • Devos, K. M., & Gale, M. D. (1997). Comparative genetics in the grasses. Plant Molecular Biology, 35, 3–15.

    Article  CAS  PubMed  Google Scholar 

  • Dharmappa, P. M., Doddaraju, P., Malagondanahalli, M. V., Rangappa, R. B., Mallikarjuna, N. M., Rajendrareddy, S. H., et al. (2019). Introgression of root and water use efficiency traits enhances water productivity: An evidence for physiological breeding in rice (Oryza sativa L.). Rice, 12(1), 14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dixit, S., Grondin, A., Lee, C. R., Henry, A., Olds, T. M., & Kumar, A. (2015). Understanding rice adaptation to varying agro-ecosystems: Trait interactions and quantitative trait loci. BMC Genetics, 16, 86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dvorak, J., Wang, L., Zhu, T., Jorgensen, C. M., Deal, K. R., Dai, X., et al. (2018). Structural variation and rates of genome evolution in the grass family seen through comparison of sequences of genomes greatly differing in size. The Plant Journal, 95, 487–503.

    Article  CAS  PubMed  Google Scholar 

  • Galindo-Castañeda, T., Brown, K. M., & Lynch, J. P. (2018). Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize. Plant, Cell and Environment, 41, 1579–1592.

    Article  CAS  PubMed  Google Scholar 

  • Gowda, V. R., Henry, A., Yamauchi, A., Shashidhar, H., & Serraj, R. (2011). Root biology and genetic improvement for drought avoidance in rice. Field Crops Research, 122, 1–13.

    Article  Google Scholar 

  • Hadebe, S. T., Modi, A. T., & Mabhaudhi, T. (2017). Drought tolerance and water use of cereal crops: A focus on sorghum as a food security crop in Sub-Saharan Africa. Journal of Agronomy and Crop Science, 203, 177–191.

    Article  CAS  Google Scholar 

  • Henry, A., Cal, A. J., Batoto, T. C., Torres, R. O., & Serraj, R. (2012). Root attributes affecting water uptake of rice (Oryza sativa) under drought. Journal of Experimental Botany, 63, 4751–4763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirabayashi, H., Sasaki, K., Kambe, T., Gannaban, R. B., Miras, M. A., Mendioro, M. S., et al. (2014). qEMF3, a novel QTL for the early-morning flowering trait from wild rice, Oryza officinalis, to mitigate heat stress damage at flowering in rice, O. sativa. Journal of Experimental Botany, 66, 1227–1236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishimaru, T., Hirabayashi, H., Ida, M., Takai, T., San-Oh, Y. A., Yoshinaga, S., et al. (2010). A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Annals of Botany, 106, 515–520.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jackson, R. B., Sperry, J. S., & Dawson, T. E. (2000). Root water uptake and transport: Using physiological processes in global predictions. Trends in Plant Science, 5, 482–488.

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo, R. E., Nord, E. A., Chimungu, J. G., Brown, K. M., & Lynch, J. P. (2013). Root cortical burden influences drought tolerance in maize. Annals of Botany, 112, 429–437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadam, N., Tamilselvan, A., Lawas, L. M. F., Quinones, C., Bahuguna, R., Thomson, M. J., et al. (2017). Genetic control of plasticity in root morphology and anatomy of rice in response to water-deficit. Plant Physiology, 174, 2302–2315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadam, N., Yin, X., Bindraban, P., Struik, P., & Jagadish, S. V. K. (2015). Does morphological and anatomical plasticity during the vegetative stage make wheat more tolerant of water-deficit stress than rice? Plant Physiology, 167, 1389–1401.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar, A., Dixit, S., Ram, T., Yadaw, R. B., Mishra, K. K., & Mandal, N. P. (2014). Breeding high-yielding drought-tolerant rice: Genetic variations and conventional and molecular approaches. Journal of Experimental Botany, 65, 6265–6278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, R., Han, Y., Lv, P., Du, R., & Liu, G. (2014). Molecular mapping of the brace root traits in sorghum (Sorghum bicolor L. Moench). Breeding Science, 64, 193–198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch, J. P. (2013). Steep, cheap and deep: An ideotype to optimize water and N acquisition by maize root systems. Annals of Botany, 112, 347–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mace, E., Singh, V., Van-Oosterom, E., Hammer, G., Hunt, C., & Jordan, D. (2012). QTL for nodal root angle in sorghum Sorghum bicolor L. Moench co-locate with QTL for traits associated with drought adaptation. Theoretical and Applied Genetics, 124, 97–109.

    Article  CAS  PubMed  Google Scholar 

  • McDonald, M. P., Galwey, N. W., & Colmer, T. D. (2002). Similarity and diversity in adventitious root anatomy as related to root aeration among a range of wetland and dryland grass species. Plant, Cell and Environment, 25, 441–451.

    Article  Google Scholar 

  • Miyamoto, N., Steudle, E., Hirasawa, T., & Lafitte, R. (2001). Hydraulic conductivity of rice roots. Journal of Experimental Botany, 52, 1835–1846.

    Article  CAS  PubMed  Google Scholar 

  • Prince, S. J., Murphy, M., Mutava, R. N., Durnell, L. A., Valliyodan, B., Shannon, J. G., et al. (2017). Root xylem plasticity to improve water use and yield in water-stressed soybean. Journal of Experimental Botany, 68, 2027–2036.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raju, B. R., Mohankumar, M. V., Sumanth, K. K., Rajanna, M. P., Udayakumar, M., Prasad, T. G., et al. (2016). Discovery of QTLs for water mining and water use efficiency traits in rice under water-limited condition through association mapping. Molecular Breeding, 36, 1–16.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ramirez-Villegas, J., Heinemann, A. B., Pereira de Castro, A., Breseghello, F., Navarro-Racines, C., Li, T., et al. (2018). Breeding implications of drought stress under future climate for upland rice in Brazil. Global Change Biology, 24, 2035–2050.

    Article  PubMed  Google Scholar 

  • Rang, Z. W., Jagadish, S. V. K., Zhou, Q. M., Craufurd, P. Q., & Heuer, S. (2011). Effect of heat and drought stress on pollen germination and spikelet fertility in rice. Environmental and Experimental Botany, 70, 58–65.

    Article  Google Scholar 

  • Reynolds, M. P., Quilligan, E., Aggarwal, P. K., Bansal, K. C., Cavalieri, A. J., Chapman, S. C., et al. (2016). An integrated approach to maintaining cereal productivity under climate change. Global Food Security, 8, 9–18.

    Article  Google Scholar 

  • Richards, R. A., & Passioura, J. B. (1989). A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments. Australian Journal of Agricultural Research, 40, 943–950.

    Article  Google Scholar 

  • Rieger, M., & Litvin, P. (1999). Root system hydraulic conductivity in species with contrasting root anatomy. Journal of Experimental Botany, 50, 201–209.

    Article  CAS  Google Scholar 

  • Sandhu, N., Raman, K. A., Torres, R. O., Audebert, A., Dardou, A., Kumar, A., et al. (2016). Rice root architectural plasticity traits and genetic regions for adaptability to variable cultivation and stress conditions. Plant Physiology, 171, 2562–2576.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scafaro, A. P., Yamori, W., Carmo-Silva, A. E., Salvucci, M. E., Von Caemmerer, S., & Atwell, B. J. (2012). Rubisco activity is associated with photosynthetic thermotolerance in a wild rice Oryza meridionalis. Physiologia Plantarum, 146, 99–109.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt, J. E., & Gaudin, A. C. (2017). Toward an integrated root ideotype for irrigated systems. Trends Plant Sciences, 22, 433–443.

    Article  CAS  Google Scholar 

  • Sengupta, S., & Majumder, A. L. (2010). Porteresia coarctata Roxb. Tateoka, a wild rice: A potential model for studying salt-stress biology in rice. Plant, Cell and Environment, 33, 526–542.

    Article  CAS  PubMed  Google Scholar 

  • Tardieu, F., Simonneau, T., & Muller, B. (2018). The physiological basis of drought tolerance in crop plants: A scenario-dependent probabilistic approach. Annual Review of Plant Biology, 69, 733–759.

    Article  CAS  PubMed  Google Scholar 

  • Tombesi, S., Johnson, R. S., Day, K. R., & DeJong, T. M. (2009). Relationships between xylem vessel characteristics, calculated axial hydraulic conductance and size-controlling capacity of peach rootstocks. Annals of Botany, 105, 327–331.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tyree, M. T., & Ewers, F. W. (1991). The hydraulic architecture of trees and other woody plants. New Phytologist, 119, 345–360.

    Article  Google Scholar 

  • Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., et al. (2013). Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45, 1097–1102.

    Article  CAS  PubMed  Google Scholar 

  • Vadez, V. (2014). Root hydraulics: The forgotten side of roots in drought adaptation. Field Crops Research, 165, 15–24.

    Article  Google Scholar 

  • Yoshida, S., & Hasegawa, S. (1982). The rice root system: its development and function. Drought resistance in crops with emphasis on rice (Vol. 10, pp. 97–134). Manila: International Rice Research Institute.

    Google Scholar 

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Acknowledgements

This work was supported by the USAID-BMGF-funded Cereal Systems Initiative for South Asia (Phase II). Partial support from The Federal Ministry for Economic Cooperation and Development, Germany (Contract No. 81141844; Project No. 11.7860.7-001.00) is also acknowledged.

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Authors and Affiliations

  1. International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines

    Raju Bheemanahalli, Sherry Hechanova, Jena K. Kshirod & S. V. Krishna Jagadish

  2. Department of Agronomy, Kansas State University, Manhattan, KS, 66506, USA

    Raju Bheemanahalli & S. V. Krishna Jagadish

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  1. Raju Bheemanahalli
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  2. Sherry Hechanova
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  4. S. V. Krishna Jagadish
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Correspondence to S. V. Krishna Jagadish.

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Bheemanahalli, R., Hechanova, S., Kshirod, J.K. et al. Root anatomical traits of wild-rices reveal links between flooded rice and dryland sorghum. Plant Physiol. Rep. 24, 155–167 (2019). https://doi.org/10.1007/s40502-019-00451-1

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