Identification, Mapping, Isolation of the Genes Resisting to Bacterial Blight and Application in Rice  

Chun Xia , Hongqi Chen , Xudong Zhu
State Key Laboratory of Rice Biology/China National Rice Research Institute, Hangzhou, 310006, P.R. China
Author    Correspondence author
Molecular Plant Breeding, 2012, Vol. 3, No. 12   doi: 10.5376/mpb.2012.03.0012
Received: 13 Sep., 2012    Accepted: 20 Sep., 2012    Published: 09 Oct., 2012
© 2012 BioPublisher Publishing Platform
This article was first published in Molecular Plant Breeding in Chinese, and here was authorized to translate and publish the paper in English under the terms of Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Xia et al., 2012, Identification, Mapping, Isolation of the Genes Resisting to Bacterial Blight and Breeding Application in Rice, Molecular Plant Breeding, Vol.3, No.12 120-130 (doi: 10.5376/mpb.2012.03.0012)

Abstract

Bacterial blight, caused by Xanthomonas oryzae pv. Oryzae, is the most devastating plant bacterial disease in Asia. Exploration, identification and utilization of new resistant germplasms to rice breeding are the effective pathway to control the disease. Mapping and cloning the resistant genes makes MAS (marker-assisted selection) and transgenic technology play a great role in breeding program for disease resistance and let people have a profound insight on molecular mechanism of resistance to bacterial blight. In this paper, mapping, cloning and application of the genes resisting to bacterial blight were summarized, and also some suggestions were put forward to relieve the damaging extent caused by bacterial blight via utilizing disease resistant breeding program.

Keywords
Rice bacterial; Gene mapping; Gene isolation; Disease resistance breeding

Bacterial blight caused by Xanthomonas oryzae pv. Oryzae, is the vascular bundle desease, and it has three common kinds: leaf blight type, wilting type and withering type. Bacterial blight broke out in many rice producing regions, such as Asia (China, Korea, Inidia, Philippines), America, North America and Australia since it was first found in Fukuoka of Japan in the 1890s. Except for Sinkiang and Gansu, bacterial blight occurred in many areas of China, especially in places near the sea, the river, the upland and easy waterlogged areas. Generally, the yield reduced 10%~30%, seriously more than 50%, and even 100% caused by this disease (Mew, 1987). Studying on genetics of resistance to bacterial blight was first carried out by Japan and IRRI, subsequently, followed by Sri Lanka, India, China and so on. Since the identification of strains Xoo used were different in different countries, scientists found that it was difficult to distinguish the resistance genes. In order to compare the identified genes, the identical differential standard was set up (Ogawa, 1993). Since the bacterial races vary continually influenced by the artificial and natural selection of genes resistance to bacterial blight, it is critical to explore and identify the new resistant resources to control the changeful races.

1 Identification of Resistance Genes to Rice Bacterial Blight
It is a long-term competitive evolutionary process between the pathogenicity of pathogenic bacteria and resistant hosts, the pathogenic bacteria will vary under stress of the resistant hosts, and the resistant hosts will react to the varied pathogenic bacteria in turn. One of the effective approaches to control the invasion of pathogenic bacteria of bacterial blight is exploring new resistant resources. As usual, the outstanding resources may be found in local varieties, wild rice varieties and artificial mutational materials. To date, 31 genes have been identified, which were located on 10 chromosomes except for Chr9 and Chr10 (Figure 1). The 6 cloned genes were identified to be resistant genes, 9 were unidentified genes, and there were 3 resistant genes from artificial mutation materials and 6 from local varieties (Nakai et al., 1998; Taura et al., 1991; Taura et al., 1992; Lee et al., 2003).

 


Figure 1 Approximate positions of the genes resisting to bacterial blight on chromosome


1.1 Unidentified genes
Mutagenesis has played a great role in enriching the resistant resources of bacterial blight and the researchers have obtained a series of new genes which were in different resistance levels and resistance specurms. So far, 9 genes, from mutagenesis and local varieties have not been identified, listed in table 1.



Table 1 Unidentified resistance genes to bacterial blight


1.2 Identified genes
Chromosome 1: Xa29(t), xa34(t), deriving from B5, a transgenic line of Oryza officinalis and BG1222, a variety from Sri Lanka, respectively. Xa29(t) was located on chromosome 1 within a 1.3 cM region flanked by RFLP markers C904 and R596. xa34(t) was defined to an interval which spans approximately 204 kb equal to 0.4 cM between the markers RM10927 and BGID25, and cosegregated with indel markers BGID34 and BGID36. Gene prediction results showed that there were no homologous proteins with the known resistance genes, indicating that a new mechanism might be performed by xa34(t) (Tan et al., 2004; Chen et al., 2011).

Chromosome 2: xa24, a new recessive gene in DV86 was identified by Mir and Khush and confirmed by Khush and Angeles. Wu et al (2008) found that xa24 was resisted to the Philippine Xoo races 4, 6, 10 and Chinese Xoo srtains Zhe173, JL691, and KS-1-21, and was mapped on chromosome 2 within a 0.14 cM region, and an approximately 71 kb in length between RM14222 and RM14226.

Chromosome 3: Xa11, resistance to Japanese Xoo races IB, II, IIIA and V, was mapped on the short arm of chromosome 3 with a genetic distance 2.0 cM and 1.0 cM from the marker RM347 and KUX11, respectively (Goto et al., 2009).

Chromosome 4: up to now, seven genes included Xa1, Xa2, Xa12, Xa14, Xa25(t), Xa30(t) and Xa31(t) have been positioned on this chromosome. Except Xa25(t), other six genes distributed on the followed six clones: OSJNBa0008M17, OSJNBa0093O08, OSJNBa0058K23,OSJNB0085C12, OSJNBa0053k19 and OSJNBa0060E08. Xa1 and Xa12 are close linkage, Xa2 is located between HZR950-5 and HRZ970-4, Xa30(t) between LOC- Os4g53060 (0.2 cM) and LOC-Os4g53120 (0.1 cM), Xa31(t) between C600 (0.1 cM) and G235 (0.1 cM), Xa14 between HZR970-8 and HZR998-1, Xa25(t) between RM6748 and RM1153, covering 19 clones containing the above six clones (Ku et al., 2008; Wang et al., 2009; Bao et al., 2010; Yoshimura et al., 1998; He et al., 2006; Gao et al., 2005).

Chromosome 5: xa5 was a recessive gene conferring resistance to bacterial blight in whole growth period from DV85, DV86, and DZ78 in Bangladesh, located on the short arm of chromosome 5 within a 0.5 cM region, about 70 kb, flanked by SNPS marker RS7 and SSR marker RM611 (Sidu et al., 1978; Blair et al., 2003).
 

Chromosome 6:
three genes, Xa7, Xa27 and xa33(t) were mapped on chromosome 6. Xa7, a dominant gene which did not mediate resistance to bacterial blight until adult-plant stage, mapped to an interval of 0.21 cM between the markers GDSSR02 and RM20593. Xa27, within a 0.052 cM region was flanked by the RFLP markers M964 and M1197 cosegregated with markers M631, M1230 and M449. RGP markers C12560S and S12715 with a genetic interval of 0.9 cM, lied outside of the RFLP markers M964 and M1197. The recombination frequency between marker G1091, and Xa7 was 8.8%, and was 22.1 cM away from marker S12715. However, Xa7 and Xa27 have different resistance spectrums to Xoo races of bacterial blight, confirming that Xa27 was not allelic to Xa7. xa33(t) was close linkage with marker RM20590, which cosegregateed with Xa7, however, the resistance characteristics were significant differ- rence between Xa7 and xa33(t) (Sidu et al., 1978; Gu et al., 2004; Korinsak et al., 2009).
Chromosome 7: xa8, a recessive gene from variety PI231129 from American, which conferred resistance or moderately resistance to Xoo races of north India with a genetic distance of 19.9 cM from marker RM214. The closer markers would be developed in future (Sidu et al., 1978; Singh et al).
Chromosome 8: xa13, a fully recessive gene originating from varieties BJ1, AC19-1-1, AUS274-1, Chinsurah Boro II and Kalimakri77-5 (Ogawa et al., 1993), which specifically confers resistance to Philippine Xoo race 6, was flanked by RFLP marker RP7 and SSR marker SR11 within a 0.84 cM interval (Chu et al., 2006).
Chromosome 11: ten resistant genes, Xa10, Xa23Xa21, Xa30(t), Xa3/Xa26, Xa22(t), Xa4, Xa32(t)Xa35(t) and Xa36(t) have been distributed on chromosome 11. Xa21, identified from Oryza rufipogon, were mapped on two clones: P0459F09 and OJ111-B01 with the genetic position of 84.6~85.7 cM on Chromosome 11, and cosegregated with RFLP marker RG103; Xa10 was mapped on clone P045F09 and its position was 85.7 cM identical with marker C189; Xa23 located between marker C189 and RM206 with the genetic distance of 0.8 cM and 1.9 cM away, respectively. The marker C1003A, the same side with marker C189, was 0.4 cM away from Xa23, covering 5 followed clones with the position from 84.6~88.4 cM with another side marker RM206: OSJNBa0072L08, OSJNBa006K21, P0480H08, OSJ- NBa0029K08 and B1356F10; Since away the marker STS03 (C1003A) with genetic distance of 2.0 cM and was more than 10 cM between the two markers: RM206 and RM224, Xa30(t) was more closed to the terminal and centromere than Xa23 and Xa3/Xa26, respectively (Ronald et al., 1992; Song et al., 1995; Yoshimura et al., 1995; Gu et al., 2008; Wang et al., 2005; Jin et al., 2007). Xa3/Xa26, Xa22(t) and Xa4 were mapped on sub clone M3H8 flanked by marker RM224 and RM114, with the genetic distance of 0 cM, 0.4 cM and 0.5 cM away RFLP marker R1056, respectively, and its position was 116.2 cM on clone OSJBa004M04 (Yang et al., 2003; Wang et al., 2003). Recently, Xa32(t), Xa35(t) and Xa36(t) were also placed on the long arm end of chromosome 11, Xa4 was likely less closed to the end than Xa36(t), because Xa4 was more 0.2 cM to the terminal marker RM224 than Xa36(t). Xa35(t), cosegerated with marker RM114, was closest to the end of long arm. Xa32(t) away the terminal marker RM5926 with the genetic of 2.6 cM may go between Xa36(t) and Xa35(t), since Xa36(t) was more 1.2 cM to RM5926 than Xa32(t) (Zheng et al., 2009; Guo et al., 2010; Miao et al., 2010).
Chromosome 12: xa32(t), steming from a new germplasm which was generated from the cross of the somatic cell of Oryza meyeriana originating from the hybrids Xishuangbanna, Yunnan, wild type and cultivared rice, was 1.7 cM away from marker RM20A (Ruan et al., 2008). Xa25(t), which confered specially resistance to PXO339 at the whole period identified from Minghui63, was located within a 9.5 cM region between NBS109 (a homologous sequences of resistance gene) and RFLP marker G1314 (Chen et al., 2002).
1.3 Unnamed genes
Two new germplasms, SH5 and SH76, which stemed from the somatic hybridization of japonica rice 8411 and Oryza meyeriana, were proved to be resistant to bacterial blight and likely to be a new gene or a new linked group (Huang et al., 2008).
2 The clone resistance genes to bacterial blight
Cloning resistant genes is the premise of knowing clearly the molecular mechanism of host resistance to bacterial blight. Bacterial blight is the mode system for studying diseases caused by pathogenic bacteria on monocotyledonous hosts. So far, 6 genes have been cloned, and two of them are recessive genes, xa5 and xa13, the others are dominant genes, Xa21, Xa1, Xa3/Xa26 and Xa27. The cloned genes are classified two categories according to their functions: expressive resistance, the expression or not of the genes plays great rolein resisting to bacterial blight (xa13 and Xa27); interactive resistance, the hosts’ expression products can interact with the proteins expressed by pathogenic bacteria (xa5, Xa21, Xa1 and Xa3/Xa26). Interestingly, the genes possessing similar functions disciplinary distribute on chromosome. xa5, xa13 and Xa27 lie on chromosome 5, 8 and 6, respectively, and only two other genes, Xa7 and xa33(t) exist on chromosome 6, However, the chromosome with Xa21, Xa1 and Xa3/Xa26 exist many other resistant genes, and these genes belong to gene cluster distribution.
2.1 Expressive resistance
xa13 isa recessive gene which confers high specially resistance to Xoo PXO99, containing five exons and encoding a protein of 307 amino acids which targets to the plasma membrane. xa13 is a promoter-mutation resistant gene, and the expression of Xa13 is the basis of pathogenic bacteria infecting to rice. The low expression of Xa13 as a result of promoter-mutation restrains pathogen infection leads to abnormal development of pollen grains and reducement of setting percentage because of its function involved in pollen development (Chu et al., 2006). In contrast to xa13, the expression of Xa27 makes a contribution to restraining invasion of pathogen bacteria.
Xa27 and avrXa27 are the first cloned pair of resistance gene corresponding to a virulence gene from rice and Xoo. Xa27 is an intronless gene and encodes protein of 113 amino acids. Xa27 with its allelic gene encodes the protein with identical sequence and expresses only in the vicinity of tissue infected by bacteria harbouring avrXa27, indicating that Xa27 works as an local defense instead of system defense. More interestingly, the intergression lines of Xa27 can mediate resistance to compatible strains of Xoo, the experiment of promoter displacement makes clear that the diverse expression is attributed to the different promoter-driven in resistant and susceptible plants (Gu et al., 2005).
2.2 Interaction resistance
2.2.1 xa5 
xa5 consisting of 4 exons and 3 introns, encodes the gamma subunit of eukaryotic transcription factor (TFIIAγ) that contains 106 amino acids. Comparing sequence between resistant and susceptible isolines reveals that an amino acid changes from valine to glutamic acid at position 39, which may result in the resistance of xa5 and the function of TFIIAγ still keeps. Sequencing TFIIAγ from resistant and susceptible cultivars shows that the amino acid at position 39 highly conserves in resistant varieties and owns two kinds of situations in susceptible varieties: Valine and Leucine (Yer et al., 2004).
2.2.2 Xa21 and Xa3/Xa26 
Xa21 encodes a protein of 1025 amino acids, which contains the extracellular NH2-terminus hydrophobic signal peptide, 23 imperfect copies of LRR, a membrane-spanning helix of hydrophobic stretch and a putative intracellular protein kinase catalytic domain. The extracellular LRR can recognize the proteins produced by avirulence gene of pathogenic bacteria, which may activate intracellular STK to withstand the invasion of pathogenic bacteria (Song et al., 1995). Study has proved that XB3 is necessary for stability of Xa21 protein and Xa21-midiated resistance, the content of Xa21 decreases along with the decree- sement of the content of XB3, so does the resistance (Wang et al., 2006). Further study also indicates that the phosphorylation active site of XB24 catalyzes the phosphorylation of some sites and slients the function of XA21 protein before inoculation. The interaction of AX21protein of Xoo and Xa21 protein makes XB24 absciss from XA21 or the reverse after inoculation so that XA21 protein works. However, the interaction of XB15 and XA21 results in dephosphorylation of XA21 protein and makes plant susceptible after inoculation (Chen et al., 2010).
Xa3/Xa26 also belongs to LRR-STK, containing 4 members, RKa, RKb, RKc, and RKd. Xa26 consists of two extrons and one intron with the length of 3 309 bp and 105 bp respectively. The amino acids of 1 103 aa consists of NH2-terminus
Signal peptide of 30 aa in length and the extracellular 26 imperfect copies of LRR, a membrane-spanning domain and a intracellular protein kinase domain (Xiang et al., 2006). Xa3 and Xa22(t), stemed from Kogyoku, a japan varietyand Zhachanglong, a Yunnan variety, were located in the same region with Xa26. The hybridization test reveals that the bands of IRBB3, Zhachanglong and Minghui63 are identical utilizing RKa of the member of Xa26 as probe. A series of analysises confirm that Xa3 and Xa26 are the same and rename as Xa3/Xa26, whether the same of Xa22(t) and Xa26 emains to verify. Xa3 was attested to possess significant difference on spectrum and resistance in different background, even turn to be a recessive character giving rise to the diversification of its name (Xa4b, Xa6 and xa9). As a whole, Xa3 works well in japonica rice (Sun et al., 2004).
2.2.3 Xa1
Xa1, confered special resistance to japan Xoo race 1 (T7174), contains 3 extrons separated by 2 introns encoding a 5406 bp ORF flanked by 5' and 3' untranslated regions of 112 and 392 bp, the derived sequence of XA1 is composed of NBS and six imperfect LRR with not distinct transmember domain. Xa1 is a particular induced gene since its expression only detected in leaves inoculated by compatible, incompatible strains and water rather than intact leaves (Yoshimura et al., 1998).
3 Application of genes resistance to bacterial blight
Improving the resistance to bacterial blight of rice utilizing the broad spectrum genes is a economic environmental and efficient method. The conventional way that makes the cross using donor and recurrent parents and sequentially backcrossing with the recurrent parent along with inoculation until 3 to 4 generation, then selfing and gaining the homozygous plants through inoculation is time-wasting, labor-consuming and difficults in pyramiding recessive genes and several genes together. The improvement of MAS, transgenesis, another culture, which combines with the conventional breeding, gradually breaks the constrains of traditional breeding.
3.1 Single-gene
In the 1980s and 1990s, Xa4 and Xa3 were the major resistance resources used in Indica rice and Japonica rice respectively. Since the loss of resistance, xa5, Xa7, Xa21 and Xa23 were put into practice recently and largely used for improving the resistance of conventional varieties, the parents of hybrid rice, and the cultivar new resistant parents of hybrid rice.
xa5, a recessive gene, expressed at the whole period. Zhongzu14, a late Indica variety and Xieyou zhong 1, a hybrid combination of Zhongzu 14 and CMS Xieqingzao A, which got through Zhejiang Province authorized committee of crop variety, were the successfully examples of pyramiding xa5 and minor genes together through MAS and anther culture (Wang et al., 2004;Ma et al., 2010).
Xa7 together with xa5 is from DV85 and mediates resistance to bacterial blight at adult-period. Kang18, Kang2 1 and Kang25 gaining from the progenies of the cross of Minghui63 and TD lines, which are the derive lines of Xa7, are severe resistant to bacterial bight (Zhou et al., 1993). Subsequently,  Kanghui63, Kanghui98 and D205, which both confer resistance to bacterial blight, were also the restorers, and the new hybrids combinations: Kangyou63, Kangyou98 and fengyou205 were cultivared and registered in Anhui, Yunnan and Jiangsu(Ding et al., 2005. Kangyou 98 were also validated in Anhui, Henan and Hunan and renamed as IIyou98 (Xu et al., 2006).
Xa21, a broad spectrum gene which stems from Oryza rufipogon with its resistance enhanced gradually from seedling stage to adult-plant stage, are wide applied to improve the parents of hybrid rice resistance to bacterial blight. The restorers, 9311, 6078, Zheda8820, Zhonghui218, R8006, R1176, Kang4183, and the male sterile, 3178S were improved or cultivated using MAS and the registered cultivars (province level and national grade) had IIyou8820, Xieyou218, Zhongyou218, Zhongyou6 (Zhong9you6 and Guodao1), Zhongyou1176, Guodao3, Shuangyou4183 (Chen et al., 2000; Tong et al., 2003; Pei et al., 2004; Cao et al., 2005; Cao et al., 2006; Luo et al., 2005).
The transgenic restorers and male sterile lines with Xa21 had Minghui63, Yanhui559, SWR20, C418, T461 and Wan21A, Peiai64S. Kangyou87, the hybrid combination of Wan21A and R18, passed the late japonica rice regional test in Anhui province (Zhou et al., 2002; Peng et al., 2001; Li et al., 2001; Ma et al., 2000; Ni et al., 2001; Rao et al., 2003; Zhao et al., 2000).
Xa23, a broad spectrum gene found from Oryza longistaminata by Zhang Qi, could rapidly become a major source resistance to bacterial blight in improving the resistance of hybrid rice since the varieties with Xa21 have been infected by some new races. Due to the short-time application, the most materials improved and cultivated by Xa23 are lines. The modified restorers and male sterile lines with Xa23 using MAS had C6201, C6271, C6351, Minghui 86, C418, HB1471, HB1473, K10, H705, H706, ZR21-sk1, Jin23 A and Zhongjia A, the combination of K10 and Funong S along with ZR21-sk1 and II-32A displayed outstanding. Moreover, the preliminary results were achieved on transgenic technology (Li et al., 2006; Xia et al., 2010; Chen et al., 2009; Zheng et al., 2009; Fan et al., 2011; Chen et al., 2009; Liu et al., 2011; Huang et al., 2009; Ji et al., 2007; Zhang et al., 2008).
3.2 Polygenic polymerization
In recent years, the varieties with genes of broad spectrum have been largely planted in various regions resulting in accelerated mutation of Xoo races. For instance, the China Xoo race VIII, infected the cultivars with Xa21. In order to strengthen resistance, broaden spectrum and prolong the resistance of varieties, pyramiding several genes into one cultivar seems to be necessary.
The genes polymerized together commonly containing 2 to 4, both the dominant genes and the recessive genes, which should broaden the spectrum and enhance the resistance of varieties to Xoo.
At present, the familiar gene polymerization combinations have Xa4/Xa21, Xa21/Xa23Xa7/Xa21, Xa4/Xa21/Xa23, Xa4/xa5/xa13/Xa21. Shuhui207 and Kanghui527 with Xa4/Xa21 were breeded (Deng et al., 2006; Huang et al., 2003; Wang et al., 2006), the hybrid rice combination Dyou17, deriving from the cross of D35 A/Kanghui 527, were through variety identification in Sichuan province. The new line R106 with Xa21/Xa23, the improved-Hua 201S lines, YR7016 and YR7023 with Xa7/Xa21 were also obtained (Luo et al., 2005; Lan et al., 2011). The lines harboring different combinations of two, three and four genes were gained and displayed highly resistance and broad spectrum (Deng et al., 2005; Yi et al., 2006; Zhou et al., 2008; Basharat et al., 2006).
Owing to the cultivars replaced rapidly and difficultly possessing perfect characters, the new hybrid combinations exists disadvantages more or less, such as susceptibility. The author analyzed the lesion length of the new hybrid combinations reacting to Xoo participated in south regional test from 2007 to 2011, the result shows that 86.5% of combinations are susceptible, 36.4% of which are susceptibe, 42% of which are moderate susceptibe, the others are moderate resistant or resistant, only Bo II you 829 t and Chun you xiang ning jing 2 tested in South China photosensitive late indica group in 2009 and the middle and lower reaches of Yangtze river for late japonica group in 2011 respectively achieved resistance level (Figure 2).
 

Figure 2 The new hybrid crosses participating in the south regional test reacting to bacterial blight from 2007 to 2011

4 Summary and prospect
The relationshiop between host and pathogenic bacteria is a process of mutual evolution. The resistant varieties released may result in changement of group members of pathogenic bacteria, either the compatible races become dominant or the present incompatible races vary.
Xa4 used in Indica rice in early stage and Xa21 largely applied in hybrid rice can be invaded successively. So it is possible that bacterial blight breaks out again under the hybrid rice widespread planted. Now the advices proposed how to alleviate the damage caused by bacterial blight are as follow:
(1) Exploring new resistant sources. Exploring the new resistant sources controlling the new infected races is the effective method since the natural law is that the new resistant sources conferring resistance to the new incompatible races must exist.
(2) Distributing the resistant cultivars reasonably. The group structure of pathogenic bacteria differs in different areas which plant cultivars with diverse background. It is pivotal to clear the genetic background of the varities, the genetic structure of bacteria population and the dynamics of races so that the efficient resistant cultivars can be released and the new effective cultivars can be replaced in time before the loss of resistance of the former since the adaptability of bacteria is produced to the local varieties in long-term evolution.
(3) Utilizing polygenic polymerization. Bacterial blight is the typical disease fitting gene-for-gene hypothesis, the products ecoded by the resistant gene in host can interact with the proteins expressed by the avr gene in incompatible races. The mutation rate occurring at several avr genes at the same time is severe low, moreover, the interaction between the resistant genes can strengthen resistance level and broaden spectrum.
(4) The research on function of Xa27 shows that the expression of Xa27 is indispensable to prevent the infection of bacteria. The plants with Xa27 of its promoter replaced can resist the compatible races, which means the scientists could create the new resistant sources using genetic engineering technology in the future.
The wide spread of hybrid rice provides the condition for rapid reproducement of Xoo. The breeding for disease resistance should be considered together with the high yield and quality to achieve the object of high yield, high efficiency, high quality, ecological and safe.
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