Translated Titles

Detection of Quantitative Trait Loci Associated with Rice Seedling Drought Tolerance Phenotypes





Key Words

水稻 ; 乾旱逆境 ; 聚乙二醇 ; 根部 ; 數量性狀基因座分析 ; 全基因體關聯性分析 ; Oryza sativa ; Drought ; PEG ; Root ; QTL analysis ; Genome-wide association study



Volume or Term/Year and Month of Publication


Academic Degree Category




Content Language


Chinese Abstract

水稻是餵養世界上一半人口的重要主食,而乾旱不論在高地或低地栽培環境下皆為顯著危害水稻產量的主要非生物逆境,特別是在未來乾旱頻率以及強度增加的趨勢下,育成耐旱水稻品種是現今必要的目標。由於植物的根部對於吸收土壤水分十分重要,根部系統結構(Root system architecture; RSA)因此被認為是乾旱耐受性中的重要性狀,根部系統結構是由許多不同的性狀共同決定,如根長、根生長角度以及根乾重等根部型態性狀。因此,為了提升水稻乾旱耐受性,針對根系進行適當的遺傳改良是具可行性的策略。本次研究採用聚乙二醇(polyethylene glycol 6000; PEG-6000)搭配水耕系統創造滲透勢壓力以模擬田間乾旱逆境,針對兩雙親本雜交族群,分別為一重組自交系(Recombinant inbred lines; RILs)和一F2族群,以及一自然種原,調查正常以及乾旱情況下的幼苗根部以及耐旱相關性狀。藉由聚乙二醇在Kimura溶液中所創造的低水勢能提供一個相對穩定的滲透勢逆境,且讓我們能針對根部相關性狀進行評估。三族群之基因型資料以測序基因分型(genotyping-by-sequencing; GBS) 技術取得單一核苷酸多型性(single nucleotide polymorphism; SNP)分子標誌。利用高密度SNP分子標誌針對各族群進行傳統的區間定位法(interval mapping; IM)、單點分析(single marker analysis; SMA)和全基因體關聯性分析(genome wide association study; GWAS),鑑定基因型和外表型的關聯。我們的定位結果顯示,針對偵測雙親本雜交族群的關聯性,使用高密度分子標誌進行單點分析可以達到區間定位法的解析度。在三個族群中共偵測到13個與根部性狀相關的染色體區間,且利用三個線上資料庫針對其中10個區間進行候選基因的探勘。根據基因功能,有一個基因被註解參與根部發育,而有三個已知基因已被證實具有調節根部生長的功能,這四個基因可以作為後續功能性分析的候選基因,以確認他們參與在根長度變化中的角色。在F2族群和自然種原中,我們偵測到數個與幼苗高度、葉捲曲程度和抽穗期相關的基因體片段。我們期望未來本研究結果所偵測到的顯著染色體片段和SNP分子標誌可應用於耐旱水稻品種之育種。

English Abstract

Rice is an important staple food feeding half of the world population. Drought as the major abiotic stress for rice greatly affects the yield production both in upland and lowland fields. In particular, with the increasing frequencies and severity of drought stress, breeding for drought-tolerant rice is necessary nowadays. Root system architecture (RSA) has been considered as a critical component in drought tolerance because of the important role of roots in water uptake from soil. Various traits contribute together to RSA, such as root morphology including root length, root growth angle and root dry weight, therefore, genetic improvement for an appropriate root system is another promising strategy to elevate drought resistance in rice. In this study, two bi-parental crosses-derived populations: a recombinant inbred lines (RILs) and a F2 population, and a diverse panel were evaluated for their root and drought-tolerant related traits at seedling stage under a hydroponic system with and without an osmotic-associated drought stress induced by polyethylene glycol 6000 (PEG-6000) treatment. Low water potential imposed by PEG in Kimura solution provided a relatively stable experimental condition and allowed us to measure the root-related traits. Single nucleotide polymorphism (SNP) markers of the three populations were obtained following the genotyping-by-sequencing (GBS) approach. With the high-density SNPs, traditional interval mapping (IM), single marker analysis (SMA), and genome wide association study (GWAS) were performed in respective population to identify the genotype-phenotype associations. Our mapping results showed the power of SMA in detecting associations in bi-parental population as compared to the resolution which simple interval mapping can achieve when using the high-density markers. Total 13 genomic regions associated with root-related traits were identified in the three populations, ten of them were searched for candidate genes using three online databases. According to the gene functions, one gene was predicted to be involved in root development and three were characterized to regulate root growth. These four genes are the candidates for future functional analysis to confirm their roles in controlling the root length. Several genomic regions associated with seedling height (SH), rolling score (RS), and heading date (HD) were detected in our F2 populations and diverse panel. We hope the significant regions and SNP markers identified in this study can be utilized in the breeding for drought-tolerant rice cultivars.

Topic Category 生物資源暨農學院 > 農藝學研究所
生物農學 > 農業
  1. Bernier, J., Kumar, A., Ramaiah, V., Spaner, D., & Atlin, G. (2007). A Large-Effect QTL for Grain Yield under Reproductive-Stage Drought Stress in Upland Rice. Crop Science, 47(2), 507–516. https://doi.org/10.2135/cropsci2006.07.0495
  2. Bradbury, P. J., Zhang, Z., Kroon, D. E., Casstevens, T. M., Ramdoss, Y., & Buckler, E. S. (2007). TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23(19), 2633–2635. https://doi.org/10.1093/bioinformatics/btm308
  3. Broman, K. W., Wu, H., Sen, S., & Churchill, G. A. (2003). R/qtl: QTL mapping in experimental crosses. Bioinformatics (Oxford, England), 19(7), 889–890. https://doi.org/10.1093/bioinformatics/btg112
  4. Chang, C. C., Chow, C. C., Tellier, L. C., Vattikuti, S., Purcell, S. M., & Lee, J. J. (2015). Second-generation PLINK: Rising to the challenge of larger and richer datasets. GigaScience, 4(1), 7. https://doi.org/10.1186/s13742-015-0047-8
  5. Choi, W.-Y., Kang, S.-Y., Park, H.-K., Kim, S.-S., Lee, K.-S., Lee, K.-S., … Choi, S.-Y. (2000). Effects of Water Stress by PEG on Growth and Physiological Traits in Rice Seedlings. KOREAN JOURNAL OF CROP SCIENCE, 45(2), 112–117.
  6. Courtois, B., Shen, L., Petalcorin, W., Carandang, S., Mauleon, R., & Li, Z. (2003). Locating QTLs controlling constitutive root traits in the rice population IAC 165 × Co39. Euphytica, 134(3), 335–345. https://doi.org/10.1023/B:EUPH.0000004987.88718.d6
  7. de Dorlodot, S., Forster, B., Pagès, L., Price, A., Tuberosa, R., & Draye, X. (2007). Root system architecture: Opportunities and constraints for genetic improvement of crops. Trends in Plant Science, 12(10), 474–481. https://doi.org/10.1016/j.tplants.2007.08.012
  8. Dempster, A. P., Laird, N. M., & Rubin, D. B. (1977). Maximum Likelihood from Incomplete Data Via the EM Algorithm. Journal of the Royal Statistical Society: Series B (Methodological), 39(1), 1–22. https://doi.org/10.1111/j.2517-6161.1977.tb01600.x
  9. Dixit, S., Singh, A., & Kumar, A. (2014). Rice Breeding for High Grain Yield under Drought: A Strategic Solution to a Complex Problem. International Journal of Agronomy. https://doi.org/10.1155/2014/863683
  10. Duan, J., & Cai, W. (2012). OsLEA3-2, an Abiotic Stress Induced Gene of Rice Plays a Key Role in Salt and Drought Tolerance. PLOS ONE, 7(9), e45117. https://doi.org/10.1371/journal.pone.0045117
  11. Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011). A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. PLOS ONE, 6(5), e19379. https://doi.org/10.1371/journal.pone.0019379
  12. Flint-Garcia, S. A., Thornsberry, J. M., & Buckler, E. S. (2003). Structure of Linkage Disequilibrium in Plants. Annual Review of Plant Biology, 54(1), 357–374. https://doi.org/10.1146/annurev.arplant.54.031902.134907
  13. Fukai, S., & Cooper, M. (1995). Development of drought-resistant cultivars using physiomorphological traits in rice. Field Crops Research, 40(2), 67–86. https://doi.org/10.1016/0378-4290(94)00096-U
  14. Fukui, H. (1982). Variability of rice production in tropical Asia. Drought Resistance in Crops with Emphasis on Rice. Retrieved from http://agris.fao.org/agris-search/search.do?recordID=US201302623151
  15. Furuta, T., Ashikari, M., Jena, K. K., Doi, K., & Reuscher, S. (2017). Adapting Genotyping-by-Sequencing for Rice F2 Populations. G3: Genes, Genomes, Genetics, 7(3), 881–893. https://doi.org/10.1534/g3.116.038190
  16. Glaubitz, J. C., Casstevens, T. M., Lu, F., Harriman, J., Elshire, R. J., Sun, Q., & Buckler, E. S. (2014). TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline. PLOS ONE, 9(2), e90346. https://doi.org/10.1371/journal.pone.0090346
  17. Grondin, A., Dixit, S., Torres, R., Venkateshwarlu, C., Rogers, E., Mitchell-Olds, T., … Henry, A. (2018). Physiological mechanisms contributing to the QTL qDTY3.2 effects on improved performance of rice Moroberekan x Swarna BC2F3:4 lines under drought. Rice, 11(1), 43. https://doi.org/10.1186/s12284-018-0234-1
  18. Hanzawa, E., Sasaki, K., Nagai, S., Obara, M., Fukuta, Y., Uga, Y., … Sato, T. (2013). Isolation of a novel mutant gene for soil-surface rooting in rice (Oryza sativa L.). Rice, 6(1), 30. https://doi.org/10.1186/1939-8433-6-30
  19. Hemamalini, G. S., Shashidhar, H. E., & Hittalmani, S. (2000). Molecular marker assisted tagging of morphological and physiological traits under two contrasting moisture regimes at peak vegetative stage in rice (Oryza sativa L.). Euphytica, 112(1), 69–78. https://doi.org/10.1023/A:1003854224905
  20. Hsu, S.-K., & Tung, C.-W. (2015). Genetic Mapping of Anaerobic Germination-Associated QTLs Controlling Coleoptile Elongation in Rice. Rice, 8(1), 38. https://doi.org/10.1186/s12284-015-0072-3
  21. Ikeda, H., Kamoshita, A., & Manabe, T. (2007). Genetic analysis of rooting ability of transplanted rice (Oryza sativa L.) under different water conditions. Journal of Experimental Botany, 58(2), 309–318. https://doi.org/10.1093/jxb/erl162
  22. Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Shibata, Y., Gomi, K., Umemura, I., … Matsuoka, M. (2005). Crown rootless1, Which Is Essential for Crown Root Formation in Rice, Is a Target of an AUXIN RESPONSE FACTOR in Auxin Signaling. The Plant Cell, 17(5), 1387–1396. https://doi.org/10.1105/tpc.105.030981
  23. Jaiswal, P., Ware, D., Ni, J., Chang, K., Zhao, W., Schmidt, S., … McCouch, S. (2002). Gramene: Development and Integration of Trait and Gene Ontologies for Rice. International Journal of Genomics. https://doi.org/10.1002/cfg.156
  24. Kato, Y., Hirotsu, S., Nemoto, K., & Yamagishi, J. (2008). Identification of QTLs controlling rice drought tolerance at seedling stage in hydroponic culture. Euphytica, 160(3), 423–430. https://doi.org/10.1007/s10681-007-9605-1
  25. Kawahara, Y., de la Bastide, M., Hamilton, J. P., Kanamori, H., McCombie, W. R., Ouyang, S., … Matsumoto, T. (2013). Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice, 6(1), 4. https://doi.org/10.1186/1939-8433-6-4
  26. Kitomi, Y., Nakao, E., Kawai, S., Kanno, N., Ando, T., Fukuoka, S., … Uga, Y. (2018). Fine Mapping of QUICK ROOTING 1 and 2, Quantitative Trait Loci Increasing Root Length in Rice. G3: Genes, Genomes, Genetics, 8(2), 727–735. https://doi.org/10.1534/g3.117.300147
  27. Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T., & Yano, M. (2002). Hd3a, a Rice Ortholog of the Arabidopsis FT Gene, Promotes Transition to Flowering Downstream of Hd1 under Short-Day Conditions. Plant and Cell Physiology, 43(10), 1096–1105. https://doi.org/10.1093/pcp/pcf156
  28. Korte, A., & Farlow, A. (2013). The advantages and limitations of trait analysis with GWAS: A review. Plant Methods, 9(1), 29. https://doi.org/10.1186/1746-4811-9-29
  29. Kumar, A., Verulkar, S., Dixit, S., Chauhan, B., Bernier, J., Venuprasad, R., … Shrivastava, M. N. (2009). Yield and yield-attributing traits of rice (Oryza sativa L.) under lowland drought and suitability of early vigor as a selection criterion. Field Crops Research, 114(1), 99–107. https://doi.org/10.1016/j.fcr.2009.07.010
  30. Lander, E. S., & Schork, N. J. (1994). Genetic dissection of complex traits. Science, 265(5181), 2037–2048. https://doi.org/10.1126/science.8091226
  31. Li, X., Guo, Z., Lv, Y., Cen, X., Ding, X., Wu, H., … Xiong, L. (2017). Genetic control of the root system in rice under normal and drought stress conditions by genome-wide association study. PLOS Genetics, 13(7), e1006889. https://doi.org/10.1371/journal.pgen.1006889
  32. Lian, G., Ding, Z., Wang, Q., Zhang, D., & Xu, J. (2014). Origins and Evolution of WUSCHEL-Related Homeobox Protein Family in Plant Kingdom. The Scientific World Journal. https://doi.org/10.1155/2014/534140
  33. Mao, C., Wang, S., Jia, Q., & Wu, P. (2006). OsEIL1, a Rice Homolog of the Arabidopsis EIN3 Regulates the Ethylene Response as a Positive Component. Plant Molecular Biology, 61(1), 141. https://doi.org/10.1007/s11103-005-6184-1
  34. Mather, K. A., Caicedo, A. L., Polato, N. R., Olsen, K. M., McCouch, S., & Purugganan, M. D. (2007). The Extent of Linkage Disequilibrium in Rice (Oryza sativa L.). Genetics, 177(4), 2223–2232. https://doi.org/10.1534/genetics.107.079616
  35. Meng, F., Xiang, D., Zhu, J., Li, Y., & Mao, C. (2019). Molecular Mechanisms of Root Development in Rice. Rice, 12(1), 1. https://doi.org/10.1186/s12284-018-0262-x
  36. Michel, B. E., & Kaufmann, M. R. (1973). The Osmotic Potential of Polyethylene Glycol 6000. Plant Physiology, 51(5), 914–916. https://doi.org/10.1104/pp.51.5.914
  37. Moncada, P., Martínez, C. P., Borrero, J., Chatel, M., Gauch Jr, H., Guimaraes, E., … McCouch, S. R. (2001). Quantitative trait loci for yield and yield components in an Oryza sativa×Oryza rufipogon BC2F2 population evaluated in an upland environment. Theoretical and Applied Genetics, 102(1), 41–52. https://doi.org/10.1007/s001220051616
  38. Money, N. P. (1989). Osmotic Pressure of Aqueous Polyethylene Glycols: Relationship between Molecular Weight and Vapor Pressure Deficit. Plant Physiology, 91(2), 766–769. https://doi.org/10.1104/pp.91.2.766
  39. Overvoorde, P., Fukaki, H., & Beeckman, T. (2010). Auxin Control of Root Development. Cold Spring Harbor Perspectives in Biology, 2(6), a001537. https://doi.org/10.1101/cshperspect.a001537
  40. Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics, 20(2), 289–290. https://doi.org/10.1093/bioinformatics/btg412
  41. Price, A., & Courtois, B. (1999). Mapping QTLs associated with drought resistance in rice: Progress, problems and prospects. Plant Growth Regulation, 29(1), 123–133. https://doi.org/10.1023/A:1006255832479
  42. Price, A. H., Steele, K. A., Moore, B. J., & Jones, R. G. W. (2002). Upland rice grown in soil-filled chambers and exposed to contrasting water-deficit regimes: II. Mapping quantitative trait loci for root morphology and distribution. Field Crops Research, 76(1), 25–43. https://doi.org/10.1016/S0378-4290(02)00010-2
  43. Price, A. H., Young, E. M., & Tomos, A. D. (1997). Quantitative trait loci associated with stomatal conductance, leaf rolling and heading date mapped in upland rice (Oryza sativa). The New Phytologist, 137(1), 83–91.
  44. Pritchard, J. K., Stephens, M., Rosenberg, N. A., & Donnelly, P. (2000). Association Mapping in Structured Populations. The American Journal of Human Genetics, 67(1), 170–181. https://doi.org/10.1086/302959
  45. Rani Debi, B., Taketa, S., & Ichii, M. (2005). Cytokinin inhibits lateral root initiation but stimulates lateral root elongation in rice (Oryza sativa). Journal of Plant Physiology, 162(5), 507–515. https://doi.org/10.1016/j.jplph.2004.08.007
  46. Salehi-Lisar, S. Y., & Bakhshayeshan-Agdam, H. (2016). Drought Stress in Plants: Causes, Consequences, and Tolerance. In Drought Stress Tolerance in Plants, Vol 1: Physiology and Biochemistry (pp. 1–16). https://doi.org/10.1007/978-3-319-28899-4_1
  47. Sasaki, A., Ashikari, M., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Swapan, D., … Matsuoka, M. (2002). A mutant gibberellin-synthesis gene in rice. Nature, 416(6882), 701. https://doi.org/10.1038/416701a
  48. Schmidt, R., Schippers, J. H. M., Mieulet, D., Watanabe, M., Hoefgen, R., Guiderdoni, E., & Mueller-Roeber, B. (2014). SALT-RESPONSIVE ERF1 Is a Negative Regulator of Grain Filling and Gibberellin-Mediated Seedling Establishment in Rice. Molecular Plant, 7(2), 404–421. https://doi.org/10.1093/mp/sst131
  49. Shin, J. H., Blay, S., McNeney, B., & Graham, J. (2006). LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. Journal of Statistical Software, 16(3), 1-10.
  50. Srividya, A., Vemireddy, L. R., Ramanarao, P. V., Sridhar, S., Jayaprada, M., Anuradha, G., … Siddiq, H. (2011). Molecular mapping of QTLs for drought related traits at seedling stage under PEG induced stress conditions in rice. American Journal of Plant Sciences, 2(2), 190–201.
  51. Steele, K. A., Virk, D. S., Kumar, R., Prasad, S. C., & Witcombe, J. R. (2007). Field evaluation of upland rice lines selected for QTLs controlling root traits. Field Crops Research, 101(2), 180–186. https://doi.org/10.1016/j.fcr.2006.11.002
  52. Sun, L., Zhang, Q., Wu, J., Zhang, L., Jiao, X., Zhang, S., … Sun, Y. (2014). Two Rice Authentic Histidine Phosphotransfer Proteins, OsAHP1 and OsAHP2, Mediate Cytokinin Signaling and Stress Responses in Rice. Plant Physiology, 165(1), 335–345. https://doi.org/10.1104/pp.113.232629
  53. Uga, Y., Assaranurak, I., Kitomi, Y., Larson, B. G., Craft, E. J., Shaff, J. E., … Kochian, L. V. (2018). Genomic regions responsible for seminal and crown root lengths identified by 2D & 3D root system image analysis. BMC Genomics, 19(1), 273. https://doi.org/10.1186/s12864-018-4639-4
  54. Uga, Y., Hanzawa, E., Nagai, S., Sasaki, K., Yano, M., & Sato, T. (2012). Identification of qSOR1, a major rice QTL involved in soil-surface rooting in paddy fields. Theoretical and Applied Genetics, 124(1), 75–86. https://doi.org/10.1007/s00122-011-1688-3
  55. Uga, Y., Kitomi, Y., Yamamoto, E., Kanno, N., Kawai, S., Mizubayashi, T., & Fukuoka, S. (2015). A QTL for root growth angle on rice chromosome 7 is involved in the genetic pathway of DEEPER ROOTING 1. Rice, 8(1), 8. https://doi.org/10.1186/s12284-015-0044-7
  56. Uga, Y., Okuno, K., & Yano, M. (2011). Dro1, a major QTL involved in deep rooting of rice under upland field conditions. Journal of Experimental Botany, 62(8), 2485–2494. https://doi.org/10.1093/jxb/erq429
  57. Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., … Yano, M. (2013a). Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45(9), 1097–1102. https://doi.org/10.1038/ng.2725
  58. Uga, Y., Yamamoto, E., Kanno, N., Kawai, S., Mizubayashi, T., & Fukuoka, S. (2013b). A major QTL controlling deep rooting on rice chromosome 4. Scientific Reports, 3, 3040. https://doi.org/10.1038/srep03040
  59. Widawsky, D. A. (1996). Prioritizing the rice research agenda for eastern India. Rice Reserch in Asia : Progress and Priorities, 109–129.
  60. Yamamoto, E., Yonemaru, J., Yamamoto, T., & Yano, M. (2012). OGRO: The Overview of functionally characterized Genes in Rice online database. Rice, 5(1), 26. https://doi.org/10.1186/1939-8433-5-26
  61. Yonemaru, J., Yamamoto, T., Fukuoka, S., Uga, Y., Hori, K., & Yano, M. (2010). Q-TARO: QTL Annotation Rice Online Database. Rice, 3(2), 194–203. https://doi.org/10.1007/s12284-010-9041-z
  62. Yu, J., Pressoir, G., Briggs, W. H., Bi, I. V., Yamasaki, M., Doebley, J. F., … Buckler, E. S. (2006). A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics, 38(2), 203. https://doi.org/10.1038/ng1702
  63. Zhang, J., Peng, Y., & Guo, Z. (2008). Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Research, 18(4), 508–521. https://doi.org/10.1038/cr.2007.104
  64. Zhang, L., Wang, S., Li, H., Deng, Q., Zheng, A., Li, S., … Wang, J. (2010). Effects of missing marker and segregation distortion on QTL mapping in F2 populations. Theoretical and Applied Genetics, 121(6), 1071–1082. https://doi.org/10.1007/s00122-010-1372-z
  65. Zhao, K., Tung, C.-W., Eizenga, G. C., Wright, M. H., Ali, M. L., Price, A. H., … McCouch, S. R. (2011). Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature Communications, 2, 467. https://doi.org/10.1038/ncomms1467
  66. Zhao, Yan, Zhang, H., Xu, J., Jiang, C., Yin, Z., Xiong, H., … Li, Z. (2018). Loci and natural alleles underlying robust roots and adaptive domestication of upland ecotype rice in aerobic conditions. PLOS Genetics, 14(8), e1007521. https://doi.org/10.1371/journal.pgen.1007521
  67. Zhao, Yu, Hu, Y., Dai, M., Huang, L., & Zhou, D.-X. (2009). The WUSCHEL-Related Homeobox Gene WOX11 Is Required to Activate Shoot-Borne Crown Root Development in Rice. The Plant Cell, 21(3), 736–748. https://doi.org/10.1105/tpc.108.061655
  68. Zhou, S., Jiang, W., Long, F., Cheng, S., Yang, W., Zhao, Y., & Zhou, D.-X. (2017). Rice Homeodomain Protein WOX11 Recruits a Histone Acetyltransferase Complex to Establish Programs of Cell Proliferation of Crown Root Meristem. The Plant Cell, 29(5), 1088–1104. https://doi.org/10.1105/tpc.16.00908
  69. Zou, G. H., Mei, H. W., Liu, H. Y., Liu, G. L., Hu, S. P., Yu, X. Q., … Luo, L. J. (2005). Grain yield responses to moisture regimes in a rice population: Association among traits and genetic markers. Theoretical and Applied Genetics, 112(1), 106–113. https://doi.org/10.1007/s00122-005-0111-3
  70. Zu, X., Lu, Y., Wang, Q., Chu, P., Miao, W., Wang, H., & La, H. (2017). A new method for evaluating the drought tolerance of upland rice cultivars. The Crop Journal, 5(6), 488–498. https://doi.org/10.1016/j.cj.2017.05.002
  71. 高景輝(2005)。植物生理分析技術。台北市:五南圖書出版股份有限公司。