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Molecular profiling of bacterial blight resistance in Malaysian rice cultivars

Perfil molecular da resistência à ferrugem bacteriana em cultivares de arroz da Malásia

Abstract

Bacteria blight is one of the most serious bacterial diseases of rice worldwide. The identification of genetic potential against bacterial blight in the existing rice resources is a prerequisite to develop multigenic resistance to combat the threat of climate change. This investigation was conducted to evaluate alleles variation in 38 Malaysian cultivars using thirteen Simple Sequences Repeats markers and one Sequence Tagged Sites (STS) marker which were reported to be linked with the resistance to bacterial blight. Based on molecular data, a dendrogram was constructed which classified the rice cultivars into seven major clusters at 0.0, 0.28 and 0.3 of similarity coefficient. Cluster 5 was the largest group comprised of ten rice cultivars where multiple genes were identified. However, xa13 could not be detected in the current rice germplasm, whereas xa2 was detected in 25 cultivars. Molecular analysis revealed that Malaysian rice cultivars possess multigenic resistance.

Keywords:
rice; genetic potential; SSR; STS; multigene resistance

Resumo

A ferrugem bacteriana é uma das doenças bacterianas mais graves do arroz em todo o mundo. A identificação do potencial genético contra a ferrugem bacteriana nos recursos de arroz existentes é um pré-requisito para desenvolver resistência multigênica no combate à ameaça da mudança climática. Esta investigação foi conduzida para avaliar a variação de alelos em 38 cultivares da Malásia usando 13 marcadores Simple Sequences Repeats (SSR) e 1 marcador Sequence Tagged Sites (STS), que foram relatados como associados à resistência à ferrugem bacteriana. Com base em dados moleculares, foi construído um dendrograma que classificou as cultivares de arroz em sete grandes agrupamentos a 0,0, 0,28 e 0,3 de coeficiente de similaridade. O Cluster 5 foi o maior grupo composto por 10 cultivares de arroz, no qual múltiplos genes foram identificados. No entanto, xa13 não pôde ser detectado no germoplasma atual de arroz, enquanto xa2 foi detectado em 25 cultivares. A análise molecular revelou que as cultivares de arroz da Malásia possuem resistência multigênica.

Palavras-chave:
arroz; potencial genético; SSR; STS; resistência multigênica

1. Introduction

Rice (Oryza sativa L) is an important staple food for over 50% of the global population. Bacteria blight caused by Xanthomonas oryzae is the most destructing bacterial disease of rice (Nino-Liu et al., 2006NIÑO-LIU, D.O., RONALD, P.C. and BOGDANOVE, A.J., 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology, vol. 7, no. 5, pp. 303-324. http://dx.doi.org/10.1111/j.1364-3703.2006.00344.x. PMid:20507449.
http://dx.doi.org/10.1111/j.1364-3703.20...
;Mew 1987MEW, T.W., 1987. Current status and future prospects of research on bacterial blight of rice. Annual Review of Phytopathology, vol. 25, no. 1, pp. 359-382. http://dx.doi.org/10.1146/annurev.py.25.090187.002043.
http://dx.doi.org/10.1146/annurev.py.25....
). The symptoms of bacterial blight in rice are characterized through drying and yellowing of leaves which usually started from the upper most tips of leaves kept proceeds downward to the petioles of leaves. Usually, the temperatures from 25-34 °C found to be favourable for the development of this disease, with median type of relative humidity above 70% (ChuKwu et al., 2019CHUKWU, S.C., RAFII, M.Y., RAMLEE, S.I., ISMAIL, S.I., HASAN, M.M., OLADOSU, Y.A., MAGAJI, U.G., AKOS, I. and OLALEKAN, K.K., 2019. Bacterial leaf blight resistance in rice: a review of conventional breeding to molecular approach. Molecular Biology Reports, vol. 46, no. 1, pp. 1519-1532. http://dx.doi.org/10.1007/s11033-019-04584-2. PMid:30628024.
http://dx.doi.org/10.1007/s11033-019-045...
) The rice crop infected by bacterial blight can lose 10-20% and even up to 80% of its yield, while major grains yield loss in the range of 2.5 to 16% in the tropics and subtropics (Dossa et al., 2020DOSSA, G.S., QUIBOD, I., ATIENZA-GRANDE, G., OLIVA, R., MAISS, E., VERA CRUZ, C. and WYDRA, K., 2020. Rice pyramided line IRBB67 (Xa4/Xa7) homeostasis under combined stress of high temperature and bacterial blight. Scientific Reports, vol. 10, no. 1, pp. 683. http://dx.doi.org/10.1038/s41598-020-57499-5. PMid:31959799.
http://dx.doi.org/10.1038/s41598-020-574...
). The disease resistance breeding programme has been found to be more effective to combat with the losses of bacterial blight in rice, while the use of Single nucleotide polymorphisms (SNPs), Next-generation sequencing (NGS) and marker assisted backcross breeding are recent advanced techniques (Chen et al., 2020CHEN, S., WANG, C., YANG, J., CHEN, B., WANG, W., SU, J., FENG, A., ZENG, L. and ZHU, X., 2020. Identification of the novel bacterial blight resistance gene Xa46 (t) by mapping and expression analysis of the rice mutant H120. Scientific Reports, vol. 10, no. 1, pp. 12642. http://dx.doi.org/10.1038/s41598-020-69639-y. PMid:32724216.
http://dx.doi.org/10.1038/s41598-020-696...
; Jamaloddin et al., 2020JAMALODDIN, M., DURGA RANI, C.V., SWATHI, G., ANURADHA, C., VANISRI, S., RAJAN, C.P.D., KRISHNAM RAJU, S., BHUVANESHWARI, V., JAGADEESWAR, R., LAHA, G.S., PRASAD, M.S., SATYANARAYANA, P.V., CHERALU, C., RAJANI, G., RAMPRASAD, E., SRAVANTHI, P., ARUN PREM KUMAR, N., ARUNA KUMARI, K., YAMINI, K.N., MAHESH, D., SANJEEV RAO, D., SUNDARAM, R.M. and MADHAV, M.S., 2020. Marker Assisted Gene Pyramiding (MAGP) for bacterial blight and blast resistance into mega rice variety “Tellahamsa”. PLoS One, vol. 15, no. 6, pp. e0234088. http://dx.doi.org/10.1371/journal.pone.0234088. PMid:32559183.
http://dx.doi.org/10.1371/journal.pone.0...
; Kumar et al., 2019KUMAR, M., SINGH, R.P., SINGH, O.N., SINGH, P., ARSODE, P., JENA, D., SAMANTARAY, S. and VERMA, R., 2019. Generation mean analysis for bacterial blight resistance and yield traits in rice. Journal of Pharmacognosy and Phytochemistry, vol. 8, no. 4, pp. 2120-2124.). The modern omics techniques and approaches including the genomics, proteomics, transcriptomics, interactomics, metabolomics, etc. may be most helpful techniques for the identification of desired genes along with their products, usually involved the pathogen perception through host as well as response which is manifested from the host against all types of pathogenic attacks in crop plants (Kumar et al., 2020KUMAR, A., KUMAR, R., SENGUPTA, D., DAS, S.N., PANDEY, M.K., BOHRA, A., SHARMA, N.K., SINHA, P., SK, H., GHAZI, I.A., LAHA, G.S. and SUNDARAM, R.M., 2020. Deployment of genetic and genomic tools toward gaining a better understanding of rice-xanthomonas oryzae pv. oryzae interactions for development of durable bacterial blight resistant rice. Frontiers in Plant Science, vol. 11, pp. 1152. http://dx.doi.org/10.3389/fpls.2020.01152. PMid:32849710.
http://dx.doi.org/10.3389/fpls.2020.0115...
). A CRISPR-Cas9 genome-edited Kitaake rice kit has been developed for the identification and evaluation for the efficacy of effector-binding elements (EBEs), in SWEET gene promoters while a software to predict the optimal resistance genes for bacterial blight of rice (Eom et al., 2019EOM, J.S., LUO, D., ATIENZA-GRANDE, G., YANG, J., JI, C., THI LUU, V., HUGUET-TAPIA, J.C., CHAR, S.N., LIU, B., NGUYEN, H., SCHMIDT, S.M., SZUREK, B., VERA CRUZ, C., WHITE, F.F., OLIVA, R., YANG, B. and FROMMER, W.B., 2019. Diagnostic kit for rice blight resistance. Nature Biotechnology, vol. 37, no. 11, pp. 1372-1379. http://dx.doi.org/10.1038/s41587-019-0268-y. PMid:31659338.
http://dx.doi.org/10.1038/s41587-019-026...
).

The most effective and sustainable method of bacterial blight disease management is the cultivation of resistant cultivars (Habarurema et al., 2012HABARUREMA, I., ASEA, G., LAMO, J., GIBSON, P., EDEMA, R., SERE, Y. and ONASANYA, R., 2012. Genetic analysis of resistance to rice bacterial blight in Uganda. African Crop Science Journal, vol. 20, no. 1, pp. 105-112.; Yang et al., 2003YANG, Z., SUN, X., WANG, S. and ZHANG, Q., 2003. Genetic and physical mapping of a new gene for bacterial blight resistance in rice. Theoretical and Applied Genetics, vol. 106, no. 8, pp. 1467-1472. http://dx.doi.org/10.1007/s00122-003-1205-4. PMid:12750790.
http://dx.doi.org/10.1007/s00122-003-120...
). The subspecies of rice including japonica, javanica, and indica are consisted of a huge reservoir of rice germplasm which have been developed through intermingling of rice cultivars and landraces (Noreen et al., 2020NOREEN, R., KHAN, S., RABBANI, A., KANWAL, A. and UZAIR, B., 2020. Screening of different rice (Oryza sativa l.) varieties for genetic diversity and bacterial blight resistance gene. Pakistan Journal of Botany, vol. 52, no. 3, pp. 1087-1096. http://dx.doi.org/10.30848/PJB2020-3(41).
http://dx.doi.org/10.30848/PJB2020-3(41)...
). Till today, 40 genes have been identified for bacterial blight resistance (Hajira et al., 2016HAJIRA, S.K., SUNDARAM, R.M., LAHA, G.S., YUGANDER, A., BALACHANDRAN, S.M., VIRAKTAMATH, B.C., SUJATHA, K., BALACHIRANJEEVI, C.H., PRANATHI, K., ANILA, M., BHASKAR, S., ABHILASH, V., MAHADEVASWAMY, H.K., KOUSIK, M., KUMAR, T.D., HARIKA, G. and REKHA, G., 2016. A single-tube, functional markerbased multiplex PCR assay for simultaneous detection of major bacterial blight resistance genes xa21, xa13 and xa5 in Rice. Rice Science, vol. 23, no. 3, pp. 144-151. http://dx.doi.org/10.1016/j.rsci.2015.11.004.
http://dx.doi.org/10.1016/j.rsci.2015.11...
). Several genes (xa4, xa5, xa7, xa13 and xa21) have been cloned and identified to produce novel cultivars that are resistant to bacterial blight (Perumalsamy et al., 2010PERUMALSAMY, S., BHARAN, M., SUDHA, M., NAGARAJAN, P., ARUL, L., SARASWATHI, R., BALASUBRAMANIAN, P. and RAMALINGAM, J., 2010. Functional marker-assisted selection for bacterial leaf blight resistance genes in rice (Oryza sativa L.). Plant Breeding, vol. 129, no. 4, pp. 400-406. http://dx.doi.org/http://dx.doi.org.
https://doi.org/http://dx.doi.orghttps:/...
). In addition, several genes such as xa2, xa4, xa7, xa30, xa33 and xa38 were found through physical mapping (Bhasin et al., 2012BHASIN, H., BHATIA, D., RAGHUVANSHI, S., LORE, J.S., SAHI, G.K., KAUR, B., VIKAL, Y. and SINGH, K., 2012. New PCR-based sequence-tagged site marker for bacterial blight resistance gene xa38 of rice. Molecular Breeding, vol. 30, no. 1, pp. 607-611. http://dx.doi.org/10.1007/s11032-011-9646-y.
http://dx.doi.org/10.1007/s11032-011-964...
; Cheema et al., 2008CHEEMA, K.K., GREWAL, N.K., VIKAL, Y., SHARMA, R., LORE, J.S., DAS, A., BHATIA, D., MAHAJAN, R., GUPTA, V., BHARAJ, T.S. and SINGH, K., 2008. A novel bacterial blight resistance gene from Oryza nivara mapped to 38 kb region on chromosome 4L and transferred to Oryza sativa L. Genetics Research, vol. 90, no. 5, pp. 397-407. http://dx.doi.org/10.1017/S0016672308009786. PMid:19061530.
http://dx.doi.org/10.1017/S0016672308009...
; Nino-Liu et al., 2006NIÑO-LIU, D.O., RONALD, P.C. and BOGDANOVE, A.J., 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology, vol. 7, no. 5, pp. 303-324. http://dx.doi.org/10.1111/j.1364-3703.2006.00344.x. PMid:20507449.
http://dx.doi.org/10.1111/j.1364-3703.20...
; Sun et al., 2003SUN, X., YANG, Z., WANG, S. and ZHANG, Q., 2003. Identification of a 47-kb DNA fragment containing xa4, a locus for bacterial blight resistance in rice. Theoretical and Applied Genetics, vol. 106, no. 4, pp. 683-687. http://dx.doi.org/10.1007/s00122-002-1117-8. PMid:12595998.
http://dx.doi.org/10.1007/s00122-002-111...
; Yang et al., 2003YANG, Z., SUN, X., WANG, S. and ZHANG, Q., 2003. Genetic and physical mapping of a new gene for bacterial blight resistance in rice. Theoretical and Applied Genetics, vol. 106, no. 8, pp. 1467-1472. http://dx.doi.org/10.1007/s00122-003-1205-4. PMid:12750790.
http://dx.doi.org/10.1007/s00122-003-120...
; Song et al., 1995SONG, W.Y., WANG, G.L., CHEN, L.L., KIM, H.S., PI, L.Y., HOLSTEN, T., GARDNER, J., WANG, B., ZHAI, W.X., ZHU, L.H., FAUQUET, C. and RONALD, P.1995. A receptor kinase-like protein encoded by the rice disease resistance gene, xa21. Science, vol. 270, no. 5243, pp. 1804-1806. http://dx.doi.org/10.1126/science.270.5243.1804. PMid:8525370.
http://dx.doi.org/10.1126/science.270.52...
). In general, a single resistance gene against some race-specific pathogen is usually incorporated into the breeding programs. However, this method is not durable for long term breeding programs (Suh et al., 2009SUH, J.P., NOH, T.H., KIM, K.Y., KIM, J.J., KIM, Y.G. and JENA, K.K., 2009. Expression levels of three bacterial blight resistance genes against K3a race of Korea by molecular and phenotype analysis in japonica rice (O. sativa L.). Journal of Crop Science and Biotechnology, vol. 12, no. 3, pp. 103-108. http://dx.doi.org/10.1007/s12892-009-0103-y.
http://dx.doi.org/10.1007/s12892-009-010...
). Rice cultivars containing multiple resistance genes have been shown to deliver durable resistance against bacterial blight (Muhammad et al., 2016MUHAMMAD, S., TAHIRA, B., HAFIZ, U.F., ZULQARNAIN, H., IMAD, N., ABID, M. and MUHAMMAD, A., 2016. Molecular screening of rice (Oryza sativa L.) germplasm for Xa4, xa5 and Xa21 bacterial leaf blight (BLB) resistant genes using linked marker approach. African Journal of Biotechnology, vol. 15, no. 41, pp. 2317-2324. http://dx.doi.org/10.5897/AJB2016.15612.
http://dx.doi.org/10.5897/AJB2016.15612...
; Pradhan et al., 2015PRADHAN, S.K., NAYAK, D.K., MOHANTY, S., BEHERA, L., BARIK, S.R., PANDIT, E., LENKA, S. and ANANDAN, A., 2015. Pyramiding of three bacterial blight resistance genes for broad spectrum resistance in deepwater rice variety Jalmagna. Rice (New York, N.Y.), vol. 8, no. 1, pp. 51. http://dx.doi.org/10.1186/s12284-015-0051-8. PMid:26054243.
http://dx.doi.org/10.1186/s12284-015-005...
, Rajpurohit et al., 2011RAJPUROHIT, D., KUMAR, R., KUMAR, M., PAUL, P., AWASTHI, A., OSMAN BASHA, P., PURI, A., JHANG, T., SINGH, K. and DHALIWAL, H.S., 2011. Pyramiding of two bacterial blight resistance and a semi dwarfing gene in Type 3 Basmati using marker-assisted selection. Euphytica, vol. 178, no. 1, pp. 111-126. http://dx.doi.org/10.1007/s10681-010-0279-8.
http://dx.doi.org/10.1007/s10681-010-027...
).

Molecular marker technologies are useful tools for the identification of desirable resistance genes as well as analysis of genetic diversity in plants (Erayman et al., 2014ERAYMAN, M., İLHAN, E., GÜZEL, Y. and EREN, A.H., 2014. Transferability of SSR markers from distantly related legumes to Glycyrrhiza species. Turkish Journal of Agriculture and Forestry, vol. 38, no. 1, pp. 32-38. http://dx.doi.org/10.3906/tar-1303-47.
http://dx.doi.org/10.3906/tar-1303-47...
; Prabakaran et al., 2010PRABAKARAN, A., PARAMASIVAM, K., RAJESH, T. and RAJARAJAN, D., 2010. Molecular of rice land races using SSR markers. Electronic Journal of Plant Breeding, vol. 1, pp. 512-516.; Davierwala et al., 2001DAVIERWALA, A.P., REDDY, A.P.K., LAGU, M.D., RANJEKAR, P.K. and GUPTA, V.S., 2001. Marker assisted selection of bacterial blight resistance genes in rice. Biochemical Genetics, vol. 39, no. 7-8, pp. 261-278. http://dx.doi.org/10.1023/A:1010282732444. PMid:11590832.
http://dx.doi.org/10.1023/A:101028273244...
). The molecular genetic diversity would contribute to preserve the desired alleles variation of genes for bacterial blight resistance. Microsatellite markers would be efficient in the profiling of alleles variation of resistance genes for bacterial blight in Malaysian rice cultivars (Song et al., 2014SONG, J.Y., LEE, G.-A., CHOI, Y.-M., LEE, S., LEE, K.B., BAE, C.-H., JUNG, Y., HYUN, D.-Y., PARK, H.-J. and LEE, M.-C., 2014. Blast resistant genes distribution and resistance reaction to blast in korean landraces of rice (Oryza sativa L.). Korean Journal of Plant Resources, vol. 27, no. 6, pp. 687-700. http://dx.doi.org/10.7732/kjpr.2014.27.6.687.
http://dx.doi.org/10.7732/kjpr.2014.27.6...
). This is essential to enrich gene pool in rice germplasm which could be utilized for crop improvement. Hence, present study was focused to identify the presence of genes, linked to bacterial blight resistance, in Malaysian rice cultivars and genetic diversity analysis.

2. Materials and methods

2.1. Plant materials

A total of 38 Malaysian rice cultivars were used in this study. The seeds of these rice cultivars were collected from Malaysian Agriculture Research and Development Institute (MARDI) as given in Table 1.

Table 1
List of Malaysian rice cultivars, with year of release.

2.2. Seed germination and DNA extraction

The seeds samples were subjected to surface sterilization as described by Pradhan et al. (2014)PRADHAN, A., THAKUR, A. and SONBOIR, H.L., 2014. Response of rice (Oryza sativa) varieties to different levels of nitrogen under rainfed aerobic ecosystem. Indian Journal of Agronomy, vol. 59, no. 1, pp. 76-79.. Germinated were transferred into seedling trays. The leaves of two-week-old seedlings were used to extract the genomic DNA as described by Ikeda et al. (2001)IKEDA, N., BAUTISTA, N.S., YAMADA, T., KAMIJIMA, O. and ISHII, T., 2001. Ultra-simple DNA extraction method for marker-assisted selection using microsatellite markers in rice. Plant Molecular Biology Reporter, vol. 19, no. 1, pp. 27-32. http://dx.doi.org/10.1007/BF02824075.
http://dx.doi.org/10.1007/BF02824075...
, where liquid nitrogen is not required for DNA extraction. 0.02 g of fresh leaf tissue was used for DNA extraction. Before slicing the plant tissue, the scissors were sterilized with absolute ethanol. Sliced pieces of leaves were transferred to 1.5 ml microtube. 200 µl of TE buffer (10 mM Tris-HCI, 1 mM EDTA, pH 8.0) were added and the leaves were grounded by using a grinder. Tubes were placed in boiling water (100 ºC) for 20 minutes. 800 µl of TE buffer (10 mM Tris-HCI, 0.1 mM EDTA, pH 8.0) were added and then mixed by vortex for 25 second and centrifuged at 14000 rpm at room temperature for 3 minutes to elute the DNA products. Lastly, the supernatant was transferred to a new 1.5 ml microtube and stored at -20 ºC for further analysis.

2.3. Polymerase chain reaction

PCR reactions were carried out in a 25 µL volume containing 6 µl of Template DNA, 0.125 µl of 10 mM dNTP mix, 0.25 unit of Taq polymerase, 2.5 µl 10x Taq buffer, 2 µl of 2 µm forward and reverse primer, 2.8 µl of 25 mM MgCI2 and 11.325 µl of sterile nucleus free water. PCR amplification was performed in a gradient thermocycler programs with the initial denaturation of 94°C for 2 minutes. It was followed by 39 cycles of denaturation at 94 °C for 30 seconds, annealing temperature around 2 ºC less than TM value of the respective primers for 45 seconds, 72 °C for 90 seconds and then the final extension at 72 °C for 10 minutes. Lastly, the PCR products were held at 4°C. PCR products were kept at -20°C for further analysis.

2.4. Microsatellite selection and cluster analysis

The molecular markers were selected from the literature which were reported to be linked with the genes controlling resistance against bacterial blight in rice. The banding patterns, the band size and the numbers of bands as well as the visibility of these bands were used as criteria in the selection of thirteen Simple Sequences Repeats (SSR) markers and one Sequence Tagged Sites (STS). The description of these markers is given in Table 2.

Table 2
Description of selected molecular markers.

The banding pattern of each amplified PCR products were scored as “+” indicating the presence of resistance and “- “indicating the absence of resistance gene. The data was exported to PAST software for cluster analysis and Unweighted Pair Group Method with Arithmetic Mean (UPGMA) dendrogram (Hammer et al., 2001HAMMER, O,, HARPER, D.A.T. and RYAN, P.D., 2001 [viewed 9 September 2021]. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica [online], vol. 4, pp. 1-9. Available from: http//palaeo-electronica.org/ 2001 _1/ past/issue1-01.htm) for genetic diversity analysis. Dice coefficient subprogram in UPGMA software implemented in PAST software was used to categorize the Malaysian rice cultivars for the resistance potential of each cultivar. The different levels of resistance in the rice cultivars were reported in the form of phylogenetic tree. PIC analyses were performed using PIC calculator software.

3. Results and discussion

Cluster analysis was used to identify the genetic relationship among the rice cultivars. Various patterns of resistance against bacterial blight were observed in the rice cultivars (Figure 1). This dendrogram was constructed based on Nei’s genetic distance. UPGMA dendrogram separates 38 germplasm into two major clusters. The genetic distance between the rice cultivars pairs was calculated based on the dice coefficient from combined data for 14 primers, ranged from 0 to 1 (Nei, 1972NEI, M., 1972. Genetic distance between populations. American Naturalist, vol. 106, no. 949, pp. 283-292. http://dx.doi.org/10.1086/282771.
http://dx.doi.org/10.1086/282771...
). The genetic similarity among the pair-wise is ranged from 0.00 to 0.91 with an average of 0.39 among the rice varieties. Result of genetic similarity showed the presence of broad range of genetic variability in Malaysian rice cultivars at the molecular level. Rice cultivars with similar disease resistant patterns were clustered into the same group and it is useful for exploitation of desired alleles variation in Malaysian rice (Song et al. 2014SONG, J.Y., LEE, G.-A., CHOI, Y.-M., LEE, S., LEE, K.B., BAE, C.-H., JUNG, Y., HYUN, D.-Y., PARK, H.-J. and LEE, M.-C., 2014. Blast resistant genes distribution and resistance reaction to blast in korean landraces of rice (Oryza sativa L.). Korean Journal of Plant Resources, vol. 27, no. 6, pp. 687-700. http://dx.doi.org/10.7732/kjpr.2014.27.6.687.
http://dx.doi.org/10.7732/kjpr.2014.27.6...
).

Figure 1
UPGMA dendrogram showed the patterns of resistance to bacterial blight in Malaysia rice varieties, based on scoring of 13 SSR and 1 STS.

Based on the dendrogram result, the cophenetic correlation coefficient is 0.778 for binary fission for presence and absence of resistance in 38 rice cultivars. High cophenetic correlation coefficient indicates that closed relationship between the matrix binary data and the dendrogram constructed. Cluster and dendrogram constructed were robust as the cophenetic correlation coefficient is very high (Mayer et al., 2010MAYER, L., DA SILVA, W.P., MOURA, A.B. and VENDRUSCOLO, C.T., 2010. AFLP analysis of Xanthomonas axonopodis and X. arboricola strains used in xanthan production studies reveal high level of polymorphism. Brazilian Journal of Microbiology, vol. 41, no. 3, pp. 741-748. http://dx.doi.org/10.1590/S1517-83822010000300026. PMid:24031551.
http://dx.doi.org/10.1590/S1517-83822010...
). Rice cultivars were grouped using unweighted pair group method with arithmetic means. High level of genetic similarity indicated that having the closed relationship between the rice cultivars pairs. It provides information to identify the genetic diversity among the rice cultivars (Khan et al., 2015KHAN, M.W., ABBASI, F.M., MASOOD, M.S., RABBANI, A., ABBASI, M.F., SAJID, M. and AHMAD, H., 2015. Identification of bacterial blight resistance gene xa7 in rice (Oryzae sativa L.) through STS marker. International Journal of Biosciences, vol. 6, no. 2, pp. 318-324. http://dx.doi.org/10.12692/ijb/6.2.318-324.
http://dx.doi.org/10.12692/ijb/6.2.318-3...
). The results also provide the baseline in the understanding the relationship between the resistance genes and Malaysian cultivars. The dendrogram indicated that rice genotypes had similar banding pattern were grouped in the same cluster. Genotypes having the large value of similarity indicated narrow level of genetic distance among the genotypes. A low value of genetic similarity indicated high diversity among the cultivar pairs.

Genetic similarity among the Malaysian rice cultivars pair-wise varies from 0.00 to 0.91. Maswangi (MRQ74) possesses multiple resistance genes while MR84 and MR263 do not possess any resistance gene (Table 3). Genetic similarity between Maswangi (MRQ74) and MR84 is 0.000 which is the least level of genetic similarity (Figure 1). The presence of multiple resistance genes in Maswangi (MRQ74) would be useful for the development of durable bacterial blight resistant cultivars in breeding programs (Evamoni et al., 2014EVAMONI, F.Z., RUBEL, M.H. and HOSSAIN, M.A., 2014. Genetic variation and relatedness for BLB resistance in rice using RAPD Markers. International Journal of Innovation and Applied Studies, vol. 8, no. 1, pp. 93-106. http://dx.doi.org/10.1007/BF00222891.
http://dx.doi.org/10.1007/BF00222891...
). Rice cultivars had the high level of genetic similarity showed small genetic distance among the pair-wise. SSR and STS markers distinguish the thirty-eight rice cultivars based on genetic distance and genetic similarity. Rice genotype with low level of genetic distance was found to be closed in the dendrogram using dice coefficient method. The resistant genes for bacterial blight reported by Chen et al. (2011)CHEN, S., LIU, X., ZENG, L., OUYANG, D., YANG, J. and ZHU, X., 2011. Genetic analysis and molecular mapping of a novel recessive gene xa34 (t) for resistance against Xanthomonas oryzae pv. oryzae. Theoretical and Applied Genetics, vol. 122, no. 7, pp. 1331-1338. http://dx.doi.org/10.1007/s00122-011-1534-7. PMid:21274511.
http://dx.doi.org/10.1007/s00122-011-153...
and Hajira et al. (2016)HAJIRA, S.K., SUNDARAM, R.M., LAHA, G.S., YUGANDER, A., BALACHANDRAN, S.M., VIRAKTAMATH, B.C., SUJATHA, K., BALACHIRANJEEVI, C.H., PRANATHI, K., ANILA, M., BHASKAR, S., ABHILASH, V., MAHADEVASWAMY, H.K., KOUSIK, M., KUMAR, T.D., HARIKA, G. and REKHA, G., 2016. A single-tube, functional markerbased multiplex PCR assay for simultaneous detection of major bacterial blight resistance genes xa21, xa13 and xa5 in Rice. Rice Science, vol. 23, no. 3, pp. 144-151. http://dx.doi.org/10.1016/j.rsci.2015.11.004.
http://dx.doi.org/10.1016/j.rsci.2015.11...
could not be detected in here, using RM 230 and xa 13 promoter, respectively. The maximum and minimum frequencies of xa 2 and xa 5 were observed in the current studies, respectively (Table 3). MR84 and MR263 did not show the presence of any gene for bacterial blight resistance, whereas Maswangi showed the presence of 10 genes (Table 3). Similar studies have been reported by Sombunjitt et al. (2017)SOMBUNJITT, S., SRIWONGCHAI, T., KULEUNG, C. and HONGTRAKUL, V., 2017. Searching for and analysis of bacterial blight resistance genes from Thailand rice germplasm. Agriculture and Natural Resources (Bangkok), vol. 51, no. 5, pp. 365-375. http://dx.doi.org/10.1016/j.anres.2017.11.001.
http://dx.doi.org/10.1016/j.anres.2017.1...
, where resistance for bacterial blight was investigated in Thai rice.

Table 3
Scoring of bands of molecular markers in Malaysian rice cultivars.

Based on the UPGMA dendrogram, a total of 38 rice cultivars had been separated into seven major groups. MR84 and MR263 were grouped into Cluster 1 and Cluster 2 alone. Both cultivars do not possess any resistance genes against bacterial blight and thus no similarity was found as compared with other rice cultivars. These two cultivars exhibited the least genetic similarity index (0.00) so maximum genetic distance was observed in UPGMA dendrogram. RIA, Kadaria, MR127 and Sri Malaysia 2 were found in cluster 3 at the similarity coefficient 0.45. In this cluster, all rice cultivars showed the presence of two bacterial blight resistance genes. Cluster 4 comprised of four Malaysian rice cultivars (MR232, MR253, Malinja and MR211) at the similarity coefficient 0.35. These rice varieties also harboured 2 bacterial blight resistance genes and different types of resistance genes were found in this group as compared to the cluster 3. Cluster 5 was the largest group comprised of 10 rice cultivars (Manik, MR185, Murni, Pulut Hitam 9, Jaya, Masawangi (MRQ74), MR219, MR106, Sri Malaysia 1 and Mahsuri) at similarity coefficient 0.6. This group comprised of rice cultivars that carrying multiple resistance genes against bacterial blight. Rice cultivars in cluster 5 had maximum bacterial blight resistance gene as compared to another cluster. Cluster 6 was the second largest group comprised of nine rice cultivars. MR81, MR159, Makmur, MR167, MR123, Pulut Malaysia, Bahagia, Sekembang and Pulut Siding were grouped into cluster 6. In cluster 6, rice cultivars possessed bacterial blight resistance genes, ranged from 5 to 8. MR220. Sekencang, MR103, Masria, Setanjung, Seberang, Q50, MRM16 and Muda were grouped into cluster 7. Rice cultivars in cluster 7 had maximum four bacterial blight resistance genes. Malaysian rice germplasm were clustered based on the bacterial blight resistance genes using molecular markers. SSR markers provide the guidance to identify the suitable gene donor and recipients of the resistance genes for future rice breeding programs (Evamoni et al., 2014EVAMONI, F.Z., RUBEL, M.H. and HOSSAIN, M.A., 2014. Genetic variation and relatedness for BLB resistance in rice using RAPD Markers. International Journal of Innovation and Applied Studies, vol. 8, no. 1, pp. 93-106. http://dx.doi.org/10.1007/BF00222891.
http://dx.doi.org/10.1007/BF00222891...
). Based on UPGMA dendrogram, highest level of resistance response in Malaysian rice varieties were observed in cluster 5 and cluster 6. This information would be significant in improving the stability and resistant potential of rice cultivars. Wang et al. (2017)WANG, J., TIAN, D., GU, K., YANG, X., WANG, L., ZENG, X. and YIN, Z., 2017. Induction of Xa10-like genes in rice cultivar Nipponbare confers disease resistance to rice bacterial blight. Molecular Plant-Microbe Interactions, vol. 30, no. 6, pp. 466-477. http://dx.doi.org/10.1094/MPMI-11-16-0229-R. PMid:28304228.
http://dx.doi.org/10.1094/MPMI-11-16-022...
inducted xa10 gene in japonica rice cv Nipponbare and confirmed the resistance against bacterial blight. Current study revealed the presence of this gene in 17 Malaysian cultivars, it reflects that current Malaysian rice germplasm possesses resistance against this biotic stress. This information would be useful in pyramiding the genes of resistance in certain cultivars which are lacking resistance genes against bacterial blight e.g. MR 263 (Evamoni et al., 2014EVAMONI, F.Z., RUBEL, M.H. and HOSSAIN, M.A., 2014. Genetic variation and relatedness for BLB resistance in rice using RAPD Markers. International Journal of Innovation and Applied Studies, vol. 8, no. 1, pp. 93-106. http://dx.doi.org/10.1007/BF00222891.
http://dx.doi.org/10.1007/BF00222891...
). Basmati rice is reported to be very sensitive to bacterial blight, however Baliyan et al. (2018)BALIYAN, N., MALIK, R., RANI, R., MEHTA, K., VASHISTH, U., DHILLON, S. and BOORA, K.S., 2018. Integrating marker-assisted background analysis with foreground selection for pyramiding bacterial blight resistance genes into Basmati rice. Comptes Rendus Biologies, vol. 341, no. 1, pp. 1-8. http://dx.doi.org/10.1016/j.crvi.2017.11.003. PMid:29254884.
http://dx.doi.org/10.1016/j.crvi.2017.11...
integrated the resistance in Basmati rice by marker assisted selection.

4. Conclusion

Evaluation of alleles variation, linked to resistance genes among rice cultivars, is the essential strategy to explore the resistance potential of rice germplasm against bacterial blight. Various alleles for different bacterial blight resistance genes were detected in Malaysian rice cultivars. A dendrogram separated the 38 Malaysian rice varieties into seven major clusters at 0.0, 0.25 and 0.3 of similarity coefficient. Cluster 5 is the largest group comprised of 10 rice cultivars carrying the multiple resistance genes. Maswangi (MRQ74) would be a potential donor parent for bacterial blight resistance in Malaysian rice breeding program. Presence of resistance genes in Malaysian rice varieties would facilitate further the rice breeders to develop the resistant cultivars carrying durable resistance genes against bacterial blight. Multigene resistance is a robust strategy in the era of climate change for a sustainable food security.

References

  • BALIYAN, N., MALIK, R., RANI, R., MEHTA, K., VASHISTH, U., DHILLON, S. and BOORA, K.S., 2018. Integrating marker-assisted background analysis with foreground selection for pyramiding bacterial blight resistance genes into Basmati rice. Comptes Rendus Biologies, vol. 341, no. 1, pp. 1-8. http://dx.doi.org/10.1016/j.crvi.2017.11.003 PMid:29254884.
    » http://dx.doi.org/10.1016/j.crvi.2017.11.003
  • BHASIN, H., BHATIA, D., RAGHUVANSHI, S., LORE, J.S., SAHI, G.K., KAUR, B., VIKAL, Y. and SINGH, K., 2012. New PCR-based sequence-tagged site marker for bacterial blight resistance gene xa38 of rice. Molecular Breeding, vol. 30, no. 1, pp. 607-611. http://dx.doi.org/10.1007/s11032-011-9646-y
    » http://dx.doi.org/10.1007/s11032-011-9646-y
  • CHEEMA, K.K., GREWAL, N.K., VIKAL, Y., SHARMA, R., LORE, J.S., DAS, A., BHATIA, D., MAHAJAN, R., GUPTA, V., BHARAJ, T.S. and SINGH, K., 2008. A novel bacterial blight resistance gene from Oryza nivara mapped to 38 kb region on chromosome 4L and transferred to Oryza sativa L. Genetics Research, vol. 90, no. 5, pp. 397-407. http://dx.doi.org/10.1017/S0016672308009786 PMid:19061530.
    » http://dx.doi.org/10.1017/S0016672308009786
  • CHEN, S., LIU, X., ZENG, L., OUYANG, D., YANG, J. and ZHU, X., 2011. Genetic analysis and molecular mapping of a novel recessive gene xa34 (t) for resistance against Xanthomonas oryzae pv. oryzae. Theoretical and Applied Genetics, vol. 122, no. 7, pp. 1331-1338. http://dx.doi.org/10.1007/s00122-011-1534-7 PMid:21274511.
    » http://dx.doi.org/10.1007/s00122-011-1534-7
  • CHEN, S., TEMNYKH, S., XU, Y., CHO, Y.G. and MCCOUCH, S.R., 1997. Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theoretical and Applied Genetics, vol. 95, no. 4, pp. 553-567. http://dx.doi.org/10.1007/s001220050596
    » http://dx.doi.org/10.1007/s001220050596
  • CHEN, S., WANG, C., YANG, J., CHEN, B., WANG, W., SU, J., FENG, A., ZENG, L. and ZHU, X., 2020. Identification of the novel bacterial blight resistance gene Xa46 (t) by mapping and expression analysis of the rice mutant H120. Scientific Reports, vol. 10, no. 1, pp. 12642. http://dx.doi.org/10.1038/s41598-020-69639-y PMid:32724216.
    » http://dx.doi.org/10.1038/s41598-020-69639-y
  • CHUKWU, S.C., RAFII, M.Y., RAMLEE, S.I., ISMAIL, S.I., HASAN, M.M., OLADOSU, Y.A., MAGAJI, U.G., AKOS, I. and OLALEKAN, K.K., 2019. Bacterial leaf blight resistance in rice: a review of conventional breeding to molecular approach. Molecular Biology Reports, vol. 46, no. 1, pp. 1519-1532. http://dx.doi.org/10.1007/s11033-019-04584-2 PMid:30628024.
    » http://dx.doi.org/10.1007/s11033-019-04584-2
  • DAVIERWALA, A.P., REDDY, A.P.K., LAGU, M.D., RANJEKAR, P.K. and GUPTA, V.S., 2001. Marker assisted selection of bacterial blight resistance genes in rice. Biochemical Genetics, vol. 39, no. 7-8, pp. 261-278. http://dx.doi.org/10.1023/A:1010282732444 PMid:11590832.
    » http://dx.doi.org/10.1023/A:1010282732444
  • DOSSA, G.S., QUIBOD, I., ATIENZA-GRANDE, G., OLIVA, R., MAISS, E., VERA CRUZ, C. and WYDRA, K., 2020. Rice pyramided line IRBB67 (Xa4/Xa7) homeostasis under combined stress of high temperature and bacterial blight. Scientific Reports, vol. 10, no. 1, pp. 683. http://dx.doi.org/10.1038/s41598-020-57499-5 PMid:31959799.
    » http://dx.doi.org/10.1038/s41598-020-57499-5
  • EOM, J.S., LUO, D., ATIENZA-GRANDE, G., YANG, J., JI, C., THI LUU, V., HUGUET-TAPIA, J.C., CHAR, S.N., LIU, B., NGUYEN, H., SCHMIDT, S.M., SZUREK, B., VERA CRUZ, C., WHITE, F.F., OLIVA, R., YANG, B. and FROMMER, W.B., 2019. Diagnostic kit for rice blight resistance. Nature Biotechnology, vol. 37, no. 11, pp. 1372-1379. http://dx.doi.org/10.1038/s41587-019-0268-y PMid:31659338.
    » http://dx.doi.org/10.1038/s41587-019-0268-y
  • ERAYMAN, M., İLHAN, E., GÜZEL, Y. and EREN, A.H., 2014. Transferability of SSR markers from distantly related legumes to Glycyrrhiza species. Turkish Journal of Agriculture and Forestry, vol. 38, no. 1, pp. 32-38. http://dx.doi.org/10.3906/tar-1303-47
    » http://dx.doi.org/10.3906/tar-1303-47
  • EVAMONI, F.Z., RUBEL, M.H. and HOSSAIN, M.A., 2014. Genetic variation and relatedness for BLB resistance in rice using RAPD Markers. International Journal of Innovation and Applied Studies, vol. 8, no. 1, pp. 93-106. http://dx.doi.org/10.1007/BF00222891
    » http://dx.doi.org/10.1007/BF00222891
  • GOTO, T., MATSUMOTO, T., FURUYA, N., TSUCHIYA, K. and YOSHIMURA, A., 2009. Mapping of bacterial blight resistance gene xa11 on rice chromosome 3. Japan Agricultural Research Quarterly, vol. 43, no. 3, pp. 221-225. http://dx.doi.org/10.6090/jarq.43.221
    » http://dx.doi.org/10.6090/jarq.43.221
  • HABARUREMA, I., ASEA, G., LAMO, J., GIBSON, P., EDEMA, R., SERE, Y. and ONASANYA, R., 2012. Genetic analysis of resistance to rice bacterial blight in Uganda. African Crop Science Journal, vol. 20, no. 1, pp. 105-112.
  • HAJIRA, S.K., SUNDARAM, R.M., LAHA, G.S., YUGANDER, A., BALACHANDRAN, S.M., VIRAKTAMATH, B.C., SUJATHA, K., BALACHIRANJEEVI, C.H., PRANATHI, K., ANILA, M., BHASKAR, S., ABHILASH, V., MAHADEVASWAMY, H.K., KOUSIK, M., KUMAR, T.D., HARIKA, G. and REKHA, G., 2016. A single-tube, functional markerbased multiplex PCR assay for simultaneous detection of major bacterial blight resistance genes xa21, xa13 and xa5 in Rice. Rice Science, vol. 23, no. 3, pp. 144-151. http://dx.doi.org/10.1016/j.rsci.2015.11.004
    » http://dx.doi.org/10.1016/j.rsci.2015.11.004
  • HAMMER, O,, HARPER, D.A.T. and RYAN, P.D., 2001 [viewed 9 September 2021]. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica [online], vol. 4, pp. 1-9. Available from: http//palaeo-electronica.org/ 2001 _1/ past/issue1-01.htm
  • HE, Q., LI, D.B., ZHU, Y.S., TAN, M.P., ZHANG, D.P. and LIN, X.H., 2006. Fine mapping of Xa2, a bacterial blight resistance gene in rice. Molecular Breeding, vol. 17, no. 1, pp. 1-6. http://dx.doi.org/10.1007/s11032-005-8698-2
    » http://dx.doi.org/10.1007/s11032-005-8698-2
  • IKEDA, N., BAUTISTA, N.S., YAMADA, T., KAMIJIMA, O. and ISHII, T., 2001. Ultra-simple DNA extraction method for marker-assisted selection using microsatellite markers in rice. Plant Molecular Biology Reporter, vol. 19, no. 1, pp. 27-32. http://dx.doi.org/10.1007/BF02824075
    » http://dx.doi.org/10.1007/BF02824075
  • JAMALODDIN, M., DURGA RANI, C.V., SWATHI, G., ANURADHA, C., VANISRI, S., RAJAN, C.P.D., KRISHNAM RAJU, S., BHUVANESHWARI, V., JAGADEESWAR, R., LAHA, G.S., PRASAD, M.S., SATYANARAYANA, P.V., CHERALU, C., RAJANI, G., RAMPRASAD, E., SRAVANTHI, P., ARUN PREM KUMAR, N., ARUNA KUMARI, K., YAMINI, K.N., MAHESH, D., SANJEEV RAO, D., SUNDARAM, R.M. and MADHAV, M.S., 2020. Marker Assisted Gene Pyramiding (MAGP) for bacterial blight and blast resistance into mega rice variety “Tellahamsa”. PLoS One, vol. 15, no. 6, pp. e0234088. http://dx.doi.org/10.1371/journal.pone.0234088 PMid:32559183.
    » http://dx.doi.org/10.1371/journal.pone.0234088
  • KHAN, M.W., ABBASI, F.M., MASOOD, M.S., RABBANI, A., ABBASI, M.F., SAJID, M. and AHMAD, H., 2015. Identification of bacterial blight resistance gene xa7 in rice (Oryzae sativa L.) through STS marker. International Journal of Biosciences, vol. 6, no. 2, pp. 318-324. http://dx.doi.org/10.12692/ijb/6.2.318-324
    » http://dx.doi.org/10.12692/ijb/6.2.318-324
  • KUMAR, A., KUMAR, R., SENGUPTA, D., DAS, S.N., PANDEY, M.K., BOHRA, A., SHARMA, N.K., SINHA, P., SK, H., GHAZI, I.A., LAHA, G.S. and SUNDARAM, R.M., 2020. Deployment of genetic and genomic tools toward gaining a better understanding of rice-xanthomonas oryzae pv. oryzae interactions for development of durable bacterial blight resistant rice. Frontiers in Plant Science, vol. 11, pp. 1152. http://dx.doi.org/10.3389/fpls.2020.01152 PMid:32849710.
    » http://dx.doi.org/10.3389/fpls.2020.01152
  • KUMAR, M., SINGH, R.P., SINGH, O.N., SINGH, P., ARSODE, P., JENA, D., SAMANTARAY, S. and VERMA, R., 2019. Generation mean analysis for bacterial blight resistance and yield traits in rice. Journal of Pharmacognosy and Phytochemistry, vol. 8, no. 4, pp. 2120-2124.
  • MAYER, L., DA SILVA, W.P., MOURA, A.B. and VENDRUSCOLO, C.T., 2010. AFLP analysis of Xanthomonas axonopodis and X. arboricola strains used in xanthan production studies reveal high level of polymorphism. Brazilian Journal of Microbiology, vol. 41, no. 3, pp. 741-748. http://dx.doi.org/10.1590/S1517-83822010000300026 PMid:24031551.
    » http://dx.doi.org/10.1590/S1517-83822010000300026
  • MCCOUCH, S.R., KOCHERT, G., YU, Z.H., WANG, Z.Y., KHUSH, G.S., COFFMAN, W.R. and TANKSLEY, S.D., 1988. Molecular mapping of rice chromosomes. Theoretical and Applied Genetics, vol. 76, no. 6, pp. 815-829. http://dx.doi.org/10.1007/BF00273666 PMid:24232389.
    » http://dx.doi.org/10.1007/BF00273666
  • MEW, T.W., 1987. Current status and future prospects of research on bacterial blight of rice. Annual Review of Phytopathology, vol. 25, no. 1, pp. 359-382. http://dx.doi.org/10.1146/annurev.py.25.090187.002043
    » http://dx.doi.org/10.1146/annurev.py.25.090187.002043
  • MUHAMMAD, S., TAHIRA, B., HAFIZ, U.F., ZULQARNAIN, H., IMAD, N., ABID, M. and MUHAMMAD, A., 2016. Molecular screening of rice (Oryza sativa L.) germplasm for Xa4, xa5 and Xa21 bacterial leaf blight (BLB) resistant genes using linked marker approach. African Journal of Biotechnology, vol. 15, no. 41, pp. 2317-2324. http://dx.doi.org/10.5897/AJB2016.15612
    » http://dx.doi.org/10.5897/AJB2016.15612
  • NEI, M., 1972. Genetic distance between populations. American Naturalist, vol. 106, no. 949, pp. 283-292. http://dx.doi.org/10.1086/282771
    » http://dx.doi.org/10.1086/282771
  • NIÑO-LIU, D.O., RONALD, P.C. and BOGDANOVE, A.J., 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology, vol. 7, no. 5, pp. 303-324. http://dx.doi.org/10.1111/j.1364-3703.2006.00344.x PMid:20507449.
    » http://dx.doi.org/10.1111/j.1364-3703.2006.00344.x
  • NOREEN, R., KHAN, S., RABBANI, A., KANWAL, A. and UZAIR, B., 2020. Screening of different rice (Oryza sativa l.) varieties for genetic diversity and bacterial blight resistance gene. Pakistan Journal of Botany, vol. 52, no. 3, pp. 1087-1096. http://dx.doi.org/10.30848/PJB2020-3(41)
    » http://dx.doi.org/10.30848/PJB2020-3(41)
  • PERUMALSAMY, S., BHARAN, M., SUDHA, M., NAGARAJAN, P., ARUL, L., SARASWATHI, R., BALASUBRAMANIAN, P. and RAMALINGAM, J., 2010. Functional marker-assisted selection for bacterial leaf blight resistance genes in rice (Oryza sativa L.). Plant Breeding, vol. 129, no. 4, pp. 400-406. http://dx.doi.org/http://dx.doi.org.
    » https://doi.org/http://dx.doi.org» https://doi.org/http://dx.doi.org
  • PHA, N.T. and LAN, N.T., 2004. Marker assisted selection in rice breeding for bacterial leaf blight. Omon Rice, vol. 12, pp. 19-26.
  • PINTA, W., TOOJINDA, T., THUMMABENJAPONE, P. and SANITCHON, J., 2013. Pyramiding of blast and bacterial leaf blight resistance genes into rice cultivar RD6 using marker assisted selection. African Journal of Biotechnology, vol. 12, no. 28, pp. 4432-4438. http://dx.doi.org/10.5897/AJB12.2028
    » http://dx.doi.org/10.5897/AJB12.2028
  • PRABAKARAN, A., PARAMASIVAM, K., RAJESH, T. and RAJARAJAN, D., 2010. Molecular of rice land races using SSR markers. Electronic Journal of Plant Breeding, vol. 1, pp. 512-516.
  • PRADHAN, A., THAKUR, A. and SONBOIR, H.L., 2014. Response of rice (Oryza sativa) varieties to different levels of nitrogen under rainfed aerobic ecosystem. Indian Journal of Agronomy, vol. 59, no. 1, pp. 76-79.
  • PRADHAN, S.K., NAYAK, D.K., MOHANTY, S., BEHERA, L., BARIK, S.R., PANDIT, E., LENKA, S. and ANANDAN, A., 2015. Pyramiding of three bacterial blight resistance genes for broad spectrum resistance in deepwater rice variety Jalmagna. Rice (New York, N.Y.), vol. 8, no. 1, pp. 51. http://dx.doi.org/10.1186/s12284-015-0051-8 PMid:26054243.
    » http://dx.doi.org/10.1186/s12284-015-0051-8
  • RAJPUROHIT, D., KUMAR, R., KUMAR, M., PAUL, P., AWASTHI, A., OSMAN BASHA, P., PURI, A., JHANG, T., SINGH, K. and DHALIWAL, H.S., 2011. Pyramiding of two bacterial blight resistance and a semi dwarfing gene in Type 3 Basmati using marker-assisted selection. Euphytica, vol. 178, no. 1, pp. 111-126. http://dx.doi.org/10.1007/s10681-010-0279-8
    » http://dx.doi.org/10.1007/s10681-010-0279-8
  • SHANTI, M.L., SHENOY, V.V., LALITHA, D.G., MOHAN, K.V., PREMALATHA, P., NAVEEN, K.G., SHASHIDHAR, H.E., ZEHR, U.B. and FREEMAN, W.H., 2010. Marker-assisted breeding for resistance to bacterial leaf blight in popular cultivar and parental lines of hybrid rice. Journal of Plant Pathology, vol. 1, no. 3, pp. 495-501. http://dx.doi.org/10.4454/jpp.v92i2.194
    » http://dx.doi.org/10.4454/jpp.v92i2.194
  • SOMBUNJITT, S., SRIWONGCHAI, T., KULEUNG, C. and HONGTRAKUL, V., 2017. Searching for and analysis of bacterial blight resistance genes from Thailand rice germplasm. Agriculture and Natural Resources (Bangkok), vol. 51, no. 5, pp. 365-375. http://dx.doi.org/10.1016/j.anres.2017.11.001
    » http://dx.doi.org/10.1016/j.anres.2017.11.001
  • SONG, J.Y., LEE, G.-A., CHOI, Y.-M., LEE, S., LEE, K.B., BAE, C.-H., JUNG, Y., HYUN, D.-Y., PARK, H.-J. and LEE, M.-C., 2014. Blast resistant genes distribution and resistance reaction to blast in korean landraces of rice (Oryza sativa L.). Korean Journal of Plant Resources, vol. 27, no. 6, pp. 687-700. http://dx.doi.org/10.7732/kjpr.2014.27.6.687
    » http://dx.doi.org/10.7732/kjpr.2014.27.6.687
  • SONG, W.Y., WANG, G.L., CHEN, L.L., KIM, H.S., PI, L.Y., HOLSTEN, T., GARDNER, J., WANG, B., ZHAI, W.X., ZHU, L.H., FAUQUET, C. and RONALD, P.1995. A receptor kinase-like protein encoded by the rice disease resistance gene, xa21. Science, vol. 270, no. 5243, pp. 1804-1806. http://dx.doi.org/10.1126/science.270.5243.1804 PMid:8525370.
    » http://dx.doi.org/10.1126/science.270.5243.1804
  • SUH, J.P., NOH, T.H., KIM, K.Y., KIM, J.J., KIM, Y.G. and JENA, K.K., 2009. Expression levels of three bacterial blight resistance genes against K3a race of Korea by molecular and phenotype analysis in japonica rice (O. sativa L.). Journal of Crop Science and Biotechnology, vol. 12, no. 3, pp. 103-108. http://dx.doi.org/10.1007/s12892-009-0103-y
    » http://dx.doi.org/10.1007/s12892-009-0103-y
  • SUN, X., YANG, Z., WANG, S. and ZHANG, Q., 2003. Identification of a 47-kb DNA fragment containing xa4, a locus for bacterial blight resistance in rice. Theoretical and Applied Genetics, vol. 106, no. 4, pp. 683-687. http://dx.doi.org/10.1007/s00122-002-1117-8 PMid:12595998.
    » http://dx.doi.org/10.1007/s00122-002-1117-8
  • WANG, J., TIAN, D., GU, K., YANG, X., WANG, L., ZENG, X. and YIN, Z., 2017. Induction of Xa10-like genes in rice cultivar Nipponbare confers disease resistance to rice bacterial blight. Molecular Plant-Microbe Interactions, vol. 30, no. 6, pp. 466-477. http://dx.doi.org/10.1094/MPMI-11-16-0229-R PMid:28304228.
    » http://dx.doi.org/10.1094/MPMI-11-16-0229-R
  • WU, K.S. and TANKSLEY, S.D., 1993. Abundance, polymorphism and genetic mapping of microsatellites in rice. Molecular & General Genetics : MGG, vol. 241, no. 1-2, pp. 225-235. http://dx.doi.org/10.1007/BF00280220 PMid:7901751.
    » http://dx.doi.org/10.1007/BF00280220
  • YANG, Z., SUN, X., WANG, S. and ZHANG, Q., 2003. Genetic and physical mapping of a new gene for bacterial blight resistance in rice. Theoretical and Applied Genetics, vol. 106, no. 8, pp. 1467-1472. http://dx.doi.org/10.1007/s00122-003-1205-4 PMid:12750790.
    » http://dx.doi.org/10.1007/s00122-003-1205-4

Publication Dates

  • Publication in this collection
    16 Dec 2022
  • Date of issue
    2022

History

  • Received
    09 Sept 2021
  • Accepted
    09 Dec 2021
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