F2 Population Phenotyping for Salt Stress Tolerant Region Identification in 'Jao Khao' Rice
Keywords:
cell membrane stability; relative water content; rice; salt toleranceAbstract
Rice is susceptible to salt stress at seedling and reproductive stages. In order to identify the specific region in the genome conferring salt tolerance trait, F2 population of the Thai landrace salt tolerant variety, 'Jao Khao' and the salt susceptible line, IR29, was generated. Based on the phenotype of 'Jao Khao' under salt stress condition, it is clustered with 'Pokkali', which is the salt tolerant standard cultivar. The phenotyping of 600 F2 individuals was performed in the hydroponic system. Two-week old seedlings were treated with stepwise salt stress using NaCl solution to reach 12 dS.m-1 for 12 days. The F2 members showed a high level of distribution in salt injury score determined according to the standard salt injury evaluation system (SES), cell membrane stability (CMS), relative water content (RWC), whole plant fresh weight, plant height and root length. SES distribution tended to show the random distribution, while CMS and RWC had bimodal distribution. The whole plant fresh weight after 12 days of salt stress displayed right skewed distribution. For the plant height and root length, both values displayed normal distribution. All of the parameters show correlation to one another. SES shows the strong negative correlation with CMS (-0.9), RWC (-0.9), and whole plant fresh weight (-0.8), but it shows less negative correlation with plant height (-0.6) and root length (-0.5). This F2 population can be used to identify the salt tolerance regions from 'Jao Khao' via bulk-segregant analysis in the future.
References
Abhayawickrama, B., Gimhani, D., Kottearachchi, N., & Herath, V. (2020). Utilization of SNP-based highly saturated molecular map of a RIL population for the detection of QTLs and mining of candidate genes for salinity tolerance in rice. J Agric Sci, 15, 345 – 361.
Arikit, S., Wanchana, S., Khanthong, S., Saensuk, C., Thianthavon, T., Vanavichit, A., & Toojinda, T. (2019). QTL-seq identifies cooked grain elongation QTLs near soluble starch synthase and starch branching enzymes in rice (Oryza sativa L.). Sci Rep, 9, 1–10.
Asch, F., & Wopereis, M. C. (2001). Responses of field-grown irrigated rice cultivars to varying levels of floodwater salinity in a semi-arid environment. Field Crops Res, 70, 127–137.
Bajji, M., Kinet, J.-M., & Lutts, S. (2002). The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul, 36, 61–70.
Becker, A., Chao, D.-Y., Zhang, X., Salt, D. E., & Baxter, I. (2011). Bulk segregant analysis using single nucleotide polymorphism microarrays. PloS One, 6, e15993.
Blum, A., & Ebercon, A. (1981). Cell membrane stability as a measure of drought and heat tolerance in wheat1. Crop Sci, 21, 43–47.
Chandran, A. K. N., Kim, J.-W., Yoo, Y.-H., Park, H. L., Kim, Y.-J., Cho, M.-H., & Jung, K.-H. (2019). Transcriptome analysis of rice-seedling roots under soil–salt stress using RNA-Seq method. Plant Biotechnol Rep, 13, 567–578.
Chattopadhyay, K., Mohanty, S. K., Vijayan, J., Marndi, B. C., Sarkar, A., Molla, K. A., Chakraborty, K., Ray, S., & Sarkar, R. K. (2021). Genetic Dissection of Component Traits for Salinity Tolerance at Reproductive Stage in Rice. Plant Mol Biol Rep, 39, 386–402.
Chauhan, B. S., Jabran, K., & Mahajan, G. (2017). Rice production worldwide. Springer Nature Switzerland.
Chen, G., Liu, C., Gao, Z., Zhang, Y., Jiang, H., Zhu, L., Ren, D., Yu, L., Xu, G., & Qian, Q. (2017). OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice. Front Plant Sci, 8, 1885.
Chutimanukul, P., Saputro, T. B., Mahaprom, P., Plaimas, K., Comai, L., Buaboocha, T., Siangliw, M., Toojinda, T., & Chadchawan, S. (2021). Combining Genome and Gene Co-expression Network Analyses for the Identification of Genes Potentially Regulating Salt Tolerance in Rice. Front Plant Sci, 12:704549. doi: 10.3389/fpls.2021.704549.
Farooq, S., & Azam, F. (2006). Cell membrane stability technique for screening salt tolerant wheat genotypes. J. Plant Physiol, 163, 629–637.
Giovannoni, J. J., Wing, R. A., Ganal, M. W., & Tanksley, S. D. (1991). Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. Nucleic Acids Res, 19(23), 6553–6568.
Gregorio, G., Senadhira, D., & Mendoza, R. (1997). Screening rice for salinity tolerance. Vol. 22. IRRI discussion paper series.
Habila, S., Khunpolwattana, N., Chantarachot, T., Buaboocha, T., Comai, L., Chadchawan, S., & Pongpanich, M. (2021). Salt stress responses and SNP-based phylogenetic analysis of Thai rice landraces. Plant Genome (submitted).
Han, Y., Lv, P., Hou, S., Li, S., Ji, G., Ma, X., Du, R., & Liu, G. (2015). Combining next generation sequencing with bulked segregant analysis to fine map a stem moisture locus in sorghum (Sorghum bicolor L. Moench). PloS One, 10, e0127065.
Hoang, T. M. L., Tran, T. N., Nguyen, T. K. T., Williams, B., Wurm, P., Bellairs, S., & Mundree, S. (2016). Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy, 6, 54.
Itoh, N., Segawa, T., Tamiru, M., Abe, A., Sakamoto, S., Uemura, A., Oikawa, K., Kutsuzawa, H., Koga, H., & Imamura, T. (2019). Next-generation sequencing-based bulked segregant analysis for QTL mapping in the heterozygous species Brassica rapa. Theor Appl Genet, 132, 2913–2925.
Krishnamurthy, S., Pundir, P., Warraich, A. S., Rathor, S., Lokeshkumar, B., Singh, N. K., & Sharma, P. C. (2020). Introgressed saltol QTL lines improves the salinity tolerance in rice at seedling stage. Front Plant Sci, 11, 833.
Lei, L., Zheng, H., Bi, Y., Yang, L., Liu, H., Wang, J., Sun, J., Zhao, H., Li, X., & Li, J. (2020). Identification of a Major QTL and candidate gene analysis of salt tolerance at the bud burst stage in rice (Oryza sativa L.) using QTL-Seq and RNA-Seq. Rice, 13, 1–14.
Lekklar, C., Pongpanich, M., Suriya-Arunroj, D., Chinpongpanich, A., Tsai, H., Comai, L., Chadchawan, S., & Buaboocha, T. (2019a). Genome-wide association study for salinity tolerance at the flowering stage in a panel of rice accessions from Thailand. BMC Genomics, 20, 1–18.
Lekklar, C., Suriya-Arunroj, D., Pongpanich, M., Comai, L., Kositsup, B., Chadchawan, S., & Buaboocha, T. (2019b). Comparative genomic analysis of rice with contrasting photosynthesis and grain production under salt stress. Genes, 10, 562.
Lutts, S., Kinet, J., & Bouharmont, J. (1996). Effects of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) cultivars differing in salinity resistance. Plant Growth Regul., 19, 207–218.
Michelmore, R. W., Paran, I., & Kesseli, R. (1991). Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. PNAS, 88, 9828–9832.
Moradi, F., & Ismail, A. M. (2007). Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot, 99, 1161–1173.
Moradi, M., Dehghani, H., & Ravari, S. Z. (2021). Genetics of physiological and agronomical traits linked to salinity tolerance in tomato. Crop Pasture Sci, 72, 280–290.
Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annu Rev Plant Biol, 59, 651–681.
Naghashzadeh, M. (2014). Response of relative water content and cell membrane stability to mycorrhizal biofertilizer in maize. eJBio, 10, 68–72.
Nguyen, H. T. T., Das Bhowmik, S., Long, H., Cheng, Y., Mundree, S., & Hoang, L. T. M. (2021). Rapid Accumulation of proline enhances salinity tolerance in Australian wild rice Oryza australiensis Domin. Plants, 10, 2044.
Pearson, G. A., Ayers, A., & Eberhard, D. (1966). Relative salt tolerance of rice during germination and early seedling development. Soil Sci, 102, 151–156.
Pundir, P., Devi, A., Krishnamurthy, S., Sharma, P. C., & Vinaykumar, N. (2021). QTLs in salt rice variety CSR10 reveals salinity tolerance at reproductive stage. Acta Physiol Plant, 43, 1–15.
Rajendran, K., Tester, M., & Roy, S. J. (2009). Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ, 32, 237–249.
Sade, N., Galkin, E., & Moshelion, M. (2015). Measuring Arabidopsis, tomato and barley leaf relative water content (RWC). Bio-protoc, 5, e1451-e1451.
Shahid, M. A., Sarkhosh, A., Khan, N., Balal, R. M., Ali, S., Rossi, L., Gómez, C., Mattson, N., Nasim, W., & Garcia-Sanchez, F. (2020). Insights into the physiological and biochemical impacts of salt stress on plant growth and development. Agronomy, 10, 938.
Shobbar, M.-S., Azhari, O., Shobbar, Z.-S., Niknam, V., Askari, H., Pessarakli, M., & Ebrahimzadeh, H. (2012). Comparative analysis of some physiological responses of rice seedlings to cold, salt, and drought stresses. J Plant Nutr, 35, 1037–1052.
Sirault, X. R., James, R. A., & Furbank, R. T. (2009). A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Funct Plant Biol, 36, 970–977.
Sun, J., Yang, L., Wang, J., Liu, H., Zheng, H., Xie, D., Zhang, M., Feng, M., Jia, Y., & Zhao, H. (2018). Identification of a cold-tolerant locus in rice (Oryza sativa L.) using bulked segregant analysis with a next-generation sequencing strategy. Rice, 11, 1–12.
Thakur, V. J. S., Ponnuswamy, R., Singh, A. K., Shankar, V. G., & Srinivasa, D. (2021). Molecular tagging of Rf genes for the fertility restoration of WA-CMS system by bulk segregant analysis in rice. Indian J Genet, 81, 43–49.
Tiwari, S., Sl, K., Kumar, V., Singh, B., Rao, A., Mithra SV, A., Rai, V., Singh, A. K., & Singh, N. K. (2016). Mapping QTLs for salt tolerance in rice (Oryza sativa L.) by bulked segregant analysis of recombinant inbred lines using 50K SNP chip. PloS One, 11, e0153610.
Tragoonrung, S., Sheng, J., & Vanavichit, A. (1996). Tagging an aromatic gene in lowland rice using bulk segregant analysis. In Rice Genetics III: (In 2 Parts) (pp. 613–618). World Scientific.
Vajrabhaya, M., & Vajrabhaya, T. (1991). Somaclonal variation for salt tolerance in rice. In In: Bajaj Y.P.S. (eds) Rice. Biotechnology in Agriculture and Forestry, vol 14.. Springer. pp. 368-382.
Venuprasad, R., Dalid, C., Del Valle, M., Zhao, D., Espiritu, M., Cruz, M. S., Amante, M., Kumar, A., & Atlin, G. (2009). Identification and characterization of large-effect quantitative trait loci for grain yield under lowland drought stress in rice using bulk-segregant analysis. Theor Appl Genet, 120, 177–190.
Vikram, P., Swamy, B. M., Dixit, S., Ahmed, H., Cruz, M. S., Singh, A. K., Ye, G., & Kumar, A. (2012). Bulk segregant analysis:“An effective approach for mapping consistent-effect drought grain yield QTLs in rice”. Field Crops Res, 134, 185–192.
Wang, J., Zhu, J., Zhang, Y., Fan, F., Li, W., Wang, F., Zhong, W., Wang, C., & Yang, J. (2018). Comparative transcriptome analysis reveals molecular response to salinity stress of salt-tolerant and sensitive genotypes of indica rice at seedling stage. Sci Rep, 8, 1–13.
Wang, Z.-f., Wang, J.-f., Bao, Y.-m., Wu, Y.-y., Xuan, S., & Zhang, H.-s. (2010). Inheritance of rice seed germination ability under salt stress. Rice Sci, 17, 105–110.
Warraich, A. S., Krishnamurthy, S., Sooch, B. S., Vinaykumar, N., Dushyanthkumar, B., Bose, J., & Sharma, P. C. (2020). Rice GWAS reveals key genomic regions essential for salinity tolerance at reproductive stage. Acta Physiol Plant, 42, 1–15.
Yamane, K., Kawasaki, M., Taniguchi, M., & Miyake, H. (2008). Correlation between chloroplast ultrastructure and chlorophyll fluorescence characteristics in the leaves of rice (Oryza sativa L.) grown under salinity. Plant Prod Sci, 11, 139–145.
Yang, L., Lei, L., Li, P., Wang, J., Wang, C., Yang, F., Chen, J., Liu, H., Zheng, H., & Xin, W. (2021). Identification of Candidate Genes Conferring Cold Tolerance to Rice (Oryza sativa L.) at the Bud-Bursting Stage Using Bulk Segregant Analysis Sequencing and Linkage Mapping. Frontiers Plant Sci, 12, 402.
Yang, X., Xia, X., Zhang, Z., Nong, B., Zeng, Y., Xiong, F., Wu, Y., Gao, J., Deng, G., & Li, D. (2017). QTL mapping by whole genome re-sequencing and analysis of candidate genes for nitrogen use efficiency in rice. Frontiers Plant Sci, 8, 1634.
Yang, Z., Huang, D., Tang, W., Zheng, Y., Liang, K., Cutler, A. J., & Wu, W. (2013). Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-throughput sequencing of pooled extremes. PloS One, 8, e68433.
Yu, J., Zao, W., He, Q., Kim, T.-S., & Park, Y.-J. (2017). Genome-wide association study and gene set analysis for understanding candidate genes involved in salt tolerance at the rice seedling stage. Mol Genet Genom, 292, 1391–1403.
Zeng, L., Shannon, M. C., & Lesch, S. M. (2001). Timing of salinity stress affects rice growth and yield components. Agric Water Manag, 48, 191–206.
Zhang, Y., Ponce, K. S., Meng, L., Chakraborty, P., Zhao, Q., Guo, L., Gao, Z., Leng, Y., & Ye, G. (2020). QTL identification for salt tolerance related traits at the seedling stage in indica rice using a multi-parent advanced generation intercross (MAGIC) population. Plant Growth Regul, 92, 365–373.
Zhao, H., Zheng, Y., Bai, F., Liu, Y., Deng, S., Liu, X., & Wang, L. (2021). Bulked segregant analysis coupled with whole-genome sequencing (BSA-Seq) and identification of a novel locus, qGL3. 5, that regulates grain length. Research Square; 2021. DOI: 10.21203/rs.3.rs-263682/v1.
Arikit, S., Wanchana, S., Khanthong, S., Saensuk, C., Thianthavon, T., Vanavichit, A., & Toojinda, T. (2019). QTL-seq identifies cooked grain elongation QTLs near soluble starch synthase and starch branching enzymes in rice (Oryza sativa L.). Sci Rep, 9, 1–10.
Asch, F., & Wopereis, M. C. (2001). Responses of field-grown irrigated rice cultivars to varying levels of floodwater salinity in a semi-arid environment. Field Crops Res, 70, 127–137.
Bajji, M., Kinet, J.-M., & Lutts, S. (2002). The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul, 36, 61–70.
Becker, A., Chao, D.-Y., Zhang, X., Salt, D. E., & Baxter, I. (2011). Bulk segregant analysis using single nucleotide polymorphism microarrays. PloS One, 6, e15993.
Blum, A., & Ebercon, A. (1981). Cell membrane stability as a measure of drought and heat tolerance in wheat1. Crop Sci, 21, 43–47.
Chandran, A. K. N., Kim, J.-W., Yoo, Y.-H., Park, H. L., Kim, Y.-J., Cho, M.-H., & Jung, K.-H. (2019). Transcriptome analysis of rice-seedling roots under soil–salt stress using RNA-Seq method. Plant Biotechnol Rep, 13, 567–578.
Chattopadhyay, K., Mohanty, S. K., Vijayan, J., Marndi, B. C., Sarkar, A., Molla, K. A., Chakraborty, K., Ray, S., & Sarkar, R. K. (2021). Genetic Dissection of Component Traits for Salinity Tolerance at Reproductive Stage in Rice. Plant Mol Biol Rep, 39, 386–402.
Chauhan, B. S., Jabran, K., & Mahajan, G. (2017). Rice production worldwide. Springer Nature Switzerland.
Chen, G., Liu, C., Gao, Z., Zhang, Y., Jiang, H., Zhu, L., Ren, D., Yu, L., Xu, G., & Qian, Q. (2017). OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice. Front Plant Sci, 8, 1885.
Chutimanukul, P., Saputro, T. B., Mahaprom, P., Plaimas, K., Comai, L., Buaboocha, T., Siangliw, M., Toojinda, T., & Chadchawan, S. (2021). Combining Genome and Gene Co-expression Network Analyses for the Identification of Genes Potentially Regulating Salt Tolerance in Rice. Front Plant Sci, 12:704549. doi: 10.3389/fpls.2021.704549.
Farooq, S., & Azam, F. (2006). Cell membrane stability technique for screening salt tolerant wheat genotypes. J. Plant Physiol, 163, 629–637.
Giovannoni, J. J., Wing, R. A., Ganal, M. W., & Tanksley, S. D. (1991). Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. Nucleic Acids Res, 19(23), 6553–6568.
Gregorio, G., Senadhira, D., & Mendoza, R. (1997). Screening rice for salinity tolerance. Vol. 22. IRRI discussion paper series.
Habila, S., Khunpolwattana, N., Chantarachot, T., Buaboocha, T., Comai, L., Chadchawan, S., & Pongpanich, M. (2021). Salt stress responses and SNP-based phylogenetic analysis of Thai rice landraces. Plant Genome (submitted).
Han, Y., Lv, P., Hou, S., Li, S., Ji, G., Ma, X., Du, R., & Liu, G. (2015). Combining next generation sequencing with bulked segregant analysis to fine map a stem moisture locus in sorghum (Sorghum bicolor L. Moench). PloS One, 10, e0127065.
Hoang, T. M. L., Tran, T. N., Nguyen, T. K. T., Williams, B., Wurm, P., Bellairs, S., & Mundree, S. (2016). Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy, 6, 54.
Itoh, N., Segawa, T., Tamiru, M., Abe, A., Sakamoto, S., Uemura, A., Oikawa, K., Kutsuzawa, H., Koga, H., & Imamura, T. (2019). Next-generation sequencing-based bulked segregant analysis for QTL mapping in the heterozygous species Brassica rapa. Theor Appl Genet, 132, 2913–2925.
Krishnamurthy, S., Pundir, P., Warraich, A. S., Rathor, S., Lokeshkumar, B., Singh, N. K., & Sharma, P. C. (2020). Introgressed saltol QTL lines improves the salinity tolerance in rice at seedling stage. Front Plant Sci, 11, 833.
Lei, L., Zheng, H., Bi, Y., Yang, L., Liu, H., Wang, J., Sun, J., Zhao, H., Li, X., & Li, J. (2020). Identification of a Major QTL and candidate gene analysis of salt tolerance at the bud burst stage in rice (Oryza sativa L.) using QTL-Seq and RNA-Seq. Rice, 13, 1–14.
Lekklar, C., Pongpanich, M., Suriya-Arunroj, D., Chinpongpanich, A., Tsai, H., Comai, L., Chadchawan, S., & Buaboocha, T. (2019a). Genome-wide association study for salinity tolerance at the flowering stage in a panel of rice accessions from Thailand. BMC Genomics, 20, 1–18.
Lekklar, C., Suriya-Arunroj, D., Pongpanich, M., Comai, L., Kositsup, B., Chadchawan, S., & Buaboocha, T. (2019b). Comparative genomic analysis of rice with contrasting photosynthesis and grain production under salt stress. Genes, 10, 562.
Lutts, S., Kinet, J., & Bouharmont, J. (1996). Effects of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) cultivars differing in salinity resistance. Plant Growth Regul., 19, 207–218.
Michelmore, R. W., Paran, I., & Kesseli, R. (1991). Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. PNAS, 88, 9828–9832.
Moradi, F., & Ismail, A. M. (2007). Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot, 99, 1161–1173.
Moradi, M., Dehghani, H., & Ravari, S. Z. (2021). Genetics of physiological and agronomical traits linked to salinity tolerance in tomato. Crop Pasture Sci, 72, 280–290.
Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annu Rev Plant Biol, 59, 651–681.
Naghashzadeh, M. (2014). Response of relative water content and cell membrane stability to mycorrhizal biofertilizer in maize. eJBio, 10, 68–72.
Nguyen, H. T. T., Das Bhowmik, S., Long, H., Cheng, Y., Mundree, S., & Hoang, L. T. M. (2021). Rapid Accumulation of proline enhances salinity tolerance in Australian wild rice Oryza australiensis Domin. Plants, 10, 2044.
Pearson, G. A., Ayers, A., & Eberhard, D. (1966). Relative salt tolerance of rice during germination and early seedling development. Soil Sci, 102, 151–156.
Pundir, P., Devi, A., Krishnamurthy, S., Sharma, P. C., & Vinaykumar, N. (2021). QTLs in salt rice variety CSR10 reveals salinity tolerance at reproductive stage. Acta Physiol Plant, 43, 1–15.
Rajendran, K., Tester, M., & Roy, S. J. (2009). Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ, 32, 237–249.
Sade, N., Galkin, E., & Moshelion, M. (2015). Measuring Arabidopsis, tomato and barley leaf relative water content (RWC). Bio-protoc, 5, e1451-e1451.
Shahid, M. A., Sarkhosh, A., Khan, N., Balal, R. M., Ali, S., Rossi, L., Gómez, C., Mattson, N., Nasim, W., & Garcia-Sanchez, F. (2020). Insights into the physiological and biochemical impacts of salt stress on plant growth and development. Agronomy, 10, 938.
Shobbar, M.-S., Azhari, O., Shobbar, Z.-S., Niknam, V., Askari, H., Pessarakli, M., & Ebrahimzadeh, H. (2012). Comparative analysis of some physiological responses of rice seedlings to cold, salt, and drought stresses. J Plant Nutr, 35, 1037–1052.
Sirault, X. R., James, R. A., & Furbank, R. T. (2009). A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Funct Plant Biol, 36, 970–977.
Sun, J., Yang, L., Wang, J., Liu, H., Zheng, H., Xie, D., Zhang, M., Feng, M., Jia, Y., & Zhao, H. (2018). Identification of a cold-tolerant locus in rice (Oryza sativa L.) using bulked segregant analysis with a next-generation sequencing strategy. Rice, 11, 1–12.
Thakur, V. J. S., Ponnuswamy, R., Singh, A. K., Shankar, V. G., & Srinivasa, D. (2021). Molecular tagging of Rf genes for the fertility restoration of WA-CMS system by bulk segregant analysis in rice. Indian J Genet, 81, 43–49.
Tiwari, S., Sl, K., Kumar, V., Singh, B., Rao, A., Mithra SV, A., Rai, V., Singh, A. K., & Singh, N. K. (2016). Mapping QTLs for salt tolerance in rice (Oryza sativa L.) by bulked segregant analysis of recombinant inbred lines using 50K SNP chip. PloS One, 11, e0153610.
Tragoonrung, S., Sheng, J., & Vanavichit, A. (1996). Tagging an aromatic gene in lowland rice using bulk segregant analysis. In Rice Genetics III: (In 2 Parts) (pp. 613–618). World Scientific.
Vajrabhaya, M., & Vajrabhaya, T. (1991). Somaclonal variation for salt tolerance in rice. In In: Bajaj Y.P.S. (eds) Rice. Biotechnology in Agriculture and Forestry, vol 14.. Springer. pp. 368-382.
Venuprasad, R., Dalid, C., Del Valle, M., Zhao, D., Espiritu, M., Cruz, M. S., Amante, M., Kumar, A., & Atlin, G. (2009). Identification and characterization of large-effect quantitative trait loci for grain yield under lowland drought stress in rice using bulk-segregant analysis. Theor Appl Genet, 120, 177–190.
Vikram, P., Swamy, B. M., Dixit, S., Ahmed, H., Cruz, M. S., Singh, A. K., Ye, G., & Kumar, A. (2012). Bulk segregant analysis:“An effective approach for mapping consistent-effect drought grain yield QTLs in rice”. Field Crops Res, 134, 185–192.
Wang, J., Zhu, J., Zhang, Y., Fan, F., Li, W., Wang, F., Zhong, W., Wang, C., & Yang, J. (2018). Comparative transcriptome analysis reveals molecular response to salinity stress of salt-tolerant and sensitive genotypes of indica rice at seedling stage. Sci Rep, 8, 1–13.
Wang, Z.-f., Wang, J.-f., Bao, Y.-m., Wu, Y.-y., Xuan, S., & Zhang, H.-s. (2010). Inheritance of rice seed germination ability under salt stress. Rice Sci, 17, 105–110.
Warraich, A. S., Krishnamurthy, S., Sooch, B. S., Vinaykumar, N., Dushyanthkumar, B., Bose, J., & Sharma, P. C. (2020). Rice GWAS reveals key genomic regions essential for salinity tolerance at reproductive stage. Acta Physiol Plant, 42, 1–15.
Yamane, K., Kawasaki, M., Taniguchi, M., & Miyake, H. (2008). Correlation between chloroplast ultrastructure and chlorophyll fluorescence characteristics in the leaves of rice (Oryza sativa L.) grown under salinity. Plant Prod Sci, 11, 139–145.
Yang, L., Lei, L., Li, P., Wang, J., Wang, C., Yang, F., Chen, J., Liu, H., Zheng, H., & Xin, W. (2021). Identification of Candidate Genes Conferring Cold Tolerance to Rice (Oryza sativa L.) at the Bud-Bursting Stage Using Bulk Segregant Analysis Sequencing and Linkage Mapping. Frontiers Plant Sci, 12, 402.
Yang, X., Xia, X., Zhang, Z., Nong, B., Zeng, Y., Xiong, F., Wu, Y., Gao, J., Deng, G., & Li, D. (2017). QTL mapping by whole genome re-sequencing and analysis of candidate genes for nitrogen use efficiency in rice. Frontiers Plant Sci, 8, 1634.
Yang, Z., Huang, D., Tang, W., Zheng, Y., Liang, K., Cutler, A. J., & Wu, W. (2013). Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-throughput sequencing of pooled extremes. PloS One, 8, e68433.
Yu, J., Zao, W., He, Q., Kim, T.-S., & Park, Y.-J. (2017). Genome-wide association study and gene set analysis for understanding candidate genes involved in salt tolerance at the rice seedling stage. Mol Genet Genom, 292, 1391–1403.
Zeng, L., Shannon, M. C., & Lesch, S. M. (2001). Timing of salinity stress affects rice growth and yield components. Agric Water Manag, 48, 191–206.
Zhang, Y., Ponce, K. S., Meng, L., Chakraborty, P., Zhao, Q., Guo, L., Gao, Z., Leng, Y., & Ye, G. (2020). QTL identification for salt tolerance related traits at the seedling stage in indica rice using a multi-parent advanced generation intercross (MAGIC) population. Plant Growth Regul, 92, 365–373.
Zhao, H., Zheng, Y., Bai, F., Liu, Y., Deng, S., Liu, X., & Wang, L. (2021). Bulked segregant analysis coupled with whole-genome sequencing (BSA-Seq) and identification of a novel locus, qGL3. 5, that regulates grain length. Research Square; 2021. DOI: 10.21203/rs.3.rs-263682/v1.
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2022-01-25
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