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Review Article
 

Impact of Marker Assisted Breeding for Bacterial Blight Resistance in Rice: A Review



Hari Kesh and Prashant Kaushik
 
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ABSTRACT

Bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) is the major limiting factor in successful rice production. The disease causes around 20-30 % annual loss in rice production and under severe conditions, the yield loss goes upto 50%. The development of resistant genotypes against this disease is the most effective and economic way to control production loss rather than spraying harmful chemicals that affects the environment. In this direction, several varieties with the single resistant gene have been released for cultivation but due to continuous evolution of new pathotypes, there is a continuous breakdown of resistance against the bacterial blight disease. Although durable resistance can be attained by introducing multiple resistant genes in a single desirable genetic background. But with conventional breeding, it is challenging due to dominance and epistatic effects of disease resistance genes against bacterial blight. However, marker-assisted breeding made it possible to identify and introduce multiple genes into a desirable genetic background with rapid, recurrent parent genome recovery and with minimum linkage drag. Molecular markers play a significant role in speeding up the disease resistance breeding programs with different stages like screening, identification, mapping and cloning of disease-resistant genes y. Hereafter, in this review article the application and achievements of marker-assisted breeding in rice against bacterial blight disease was summarized.

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  How to cite this article:

Hari Kesh and Prashant Kaushik, 2020. Impact of Marker Assisted Breeding for Bacterial Blight Resistance in Rice: A Review. Plant Pathology Journal, 19: 151-165.

DOI: 10.3923/ppj.2020.151.165

URL: https://scialert.net/abstract/?doi=ppj.2020.151.165
 
Copyright: © 2020. This is an open access article distributed under the terms of the creative commons attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

INTRODUCTION

Rice is a staple food for more than 60% of the world population. Moreover, rice consumption supplies more than 20% calories requirement of the people in South East Asia. Furthermore, the rice plant parts are also used as animal feed. During the past decade, rice demand has increased from 76-763 million t and this trend is expected to continue in the near future1. The continuous supply of rice per the demand of the consumer can only be achieved by maintaining a stable rice production2. More than 90% of the rice total production is produced in Asia and China and India are the leading producer countries. In India, rice is cultivated over about 44.1 million ha area with the production of 165.3 million t and productivity3 of 3.78 t ha1.

Rice is sensitive to many stresses. In this direction, there are two broad areas of stresses, abiotic (salinity, heat, drought, cold, submergence, radiation and heavy metals) and biotic (pathogens and herbivore) factors4. Among biotic stresses, three diseases are considered to be the most devastating worldwide namely, bacterial blight caused by Xanthomonas oryzae pv. oryzae, blast by Pyricularia grisea and sheath blight by Rhizoctonia solani.5. Several preventive measures such as chemical and biological methods are used to control the spread of these disease and insect pests. Unfortunately, these measures are not very useful. The use of pesticides is expensive and are not environmental-friendly. Therefore, host –plant resistance is the most effective breeding strategy to control the biotic stress in contrast to the environmentally inimical use of pesticides6-8.

Yield potential of rice can be improved with the help of various strategies, conventional hybridization and selection procedures, ideotype breeding, heterosis breeding, wide hybridization and molecular breeding9. But all these methods employ a forward breeding approach based on traits of interest. The selection of advanced pedigree lines and recombinant inbred lines requires a long process that can take up to 8-9 years to generate elite lines for varietal release. With the development of gene identification technologies, the marker-assisted selection (MAS) technique is typically used to improve disease and insect resistance.

The scope of MAS breeding for targeted introgression of bacterial blight (BB) resistance genes10-19, blast resistance genes20-24, sheath blight25 and brown planthoppers resistance genes26-28 and gall midge29 have been successfully demonstrated30. Hence, molecular breeding offers the opportunity to increase the speed and efficiency of plant breeding. It lays the foundation for modern crop improvement in the 21st century31 and simultaneously helps to identify superior gene combinations, leading to significant disease resilience. The term molecular breeding is used collectively for several breeding strategies, such as MAS, MABC, marker-assisted recurrent selection (MARS) and genomic selection32.In this review, the application and achievements of marker-assisted breeding in rice against bacterial blight disease was summarized.

Bacterial blight disease of rice: Bacterial blight is a seed-borne disease caused by a gram-negative bacterium Xanthomonas oryzae pv. Oryzae is a severe threat to rice production33-35. The disease was first observed by the farmers of the Fukuoka area, in Kyushu prefecture36 of Japan, in 1884. Whereas, in India, the first incidence of bacterial blight disease in rice was reported in Maharashtra by Srinivasan et al.37. Earlier, the disease in India was considered to be of minor importance until it broke out in an epidemic form in Shahabad district of Bihar38 in 1963. This disease can affect rice plants at any plant growth stages. BB in Rice generally causes yield loss ranging from 20-30% 39,40. In case of severe infection, disease cause yield loss up to 50-100%41-44 besides severely affected the grain quality13,17. Due to the severe damage caused by bacterial blight disease, there is an urgent need for strategies to control this epidemic45. Breeding for disease resistance is the most effective and economical method for control of BB that has a neutral impact on the environment. Several germ plasm donors carrying assorted genes for control of BB resistance have been used to develop BB resistant varieties6.

Breeding rice varieties with multiple disease and insect resistance genes will broaden the resistance spectrum and increase durability for the commonly cultivated varieties8. Whereas, the large scale and long term cultivation of varieties with single genes may enable the pathogen to overcome BB resistance. However, this can be delayed by pyramiding multiple resistance genes into rice cultivars. The probability of simultaneous pathogen mutation for virulence to 2 or more effective genes is much lower than for a single gene. Gene pyramiding is difficult using conventional breeding methods due to the dominance and epistasis effects of genes governing disease resistance. However, the availability of molecular markers closely linked with each of the resistance genes makes the identification of plants with several disease resistance genes46. Historically, long term cultivation of rice varieties carrying resistance gene has resulted in a significant shift in pathogen-race frequency and consequent breakdown of resistance47.

An example of this is the failure of Xa4, which was incorporated widely in many high yielding varieties via conventional breeding. Widespread cultivation of varieties carrying Xa4 has led to the predominance of Xoo race that can easily overcome resistance conferred by this gene6. One tangible solution to resistance breakdown is pyramiding of multiple resistance genes in the background of modern high yielding varieties48. Xa21 gene in rice breeding program was identified from the wild rice O. longistaminata49,50. But the resistance due to the presence of this gene was recently broken down by new virulent strains in Southern and Yangtze River Valley in China51,52. When two or more genes are introgressed, phenotypic evaluation is unable to distinguish the effect of individual gene precisely since each gene confers resistance to and combats multiple races of the pathogen53.

Moreover, in the presence of a dominant and recessive allele, the effect of the recessive gene is masked54. The effectiveness of resistance genes varies over locations due to geographical structuring of the pathogen. Knowledge of the pathogen population structure and virulence characteristics is therefore essential for a successful breeding program aimed at durable resistance55.

Bacterial blight resistance genes in the rice wild relatives: During domestication process from wild species to cultivated rice, selection of desirable agronomic traits to develop varieties that are high yielding and more suitable to humankind leads to loss of many useful genes and a significant reduction of genetic diversity in rice gene pool56. The number of alleles in cultivated rice had been reduced by 50-60% as compared to wild rice57. Therefore, it is necessary, to widen the genetic base of rice through identification and introgression of novel resistance genes from wild relatives of rice to develop cultivars with resistance to Xanthomonas oryzae pv. oryzae. Wild species of rice are reservoirs of many useful genes58 but a vast majority of these genes remain untapped, because it is often difficult to identify and transfer these genes into cultivated rice. Recently, many genes resistant to diseases, insects, abiotic stress and also for high yield have been transferred from wild species of rice. Many wild species of cultivated rice such as O. longistaminata, O. rufipogon, O. minuta, O. barthii, O. brachyantha, O. granulate, O. ridleyi and O. nivara have been reported to be resistant to BB58. Khush et al.49 transferred Xa21, a dominant BB resistance gene from O. longistaminata into IR24. The F1 showed resistant to 6 races of bacterial blight in the Philippines, indicating that the resistance of O. longistaminata was dominant. Xa23, a dominant resistant gene effective at all growth stages was identified from wild rice species of Oryza rufipogon59,60. The Xa23 gene was found highly resistant to 10 Philippine races (P1-P10), 7 Chinese pathotypes (C1-C7) and 3 Japanese races (TI-T3) at maximum tillering stage61. Jin et al.62 identified a BB resistance gene Xa 30 from wild species O. rufipogon and transferred this locus to cultivated rice to breed near-isogenic lines. Tan et al.63 detected Xa 29 locus from O. officinalis and mapped within a 1.3 cM region flanked by RFLP markers on Chromosome 1. Similarly, Xa32(t) gene from Oryzae ustraliensis resistant to Xoo strains P1, P4, P5, P6, P7, P8, P9, KXO85 but susceptible to P2 and P3 was mapped by two SSR markers on the long arm64 of chromosome 11. Guo et al.65 transferred Xa35(t), a novel source of BB resistance gene from O. minuta (Acc. No. 101133) into IR24 cultivar of O. sativa L. The bacterial blight resistance genes identified in the rice wild relatives are presented in Table 1.

Genetics of bacterial blight resistance genes: To date, at least 45 genes conferring BB resistance have been reported71-77 and designated in a series from Xa1 to Xa4569,76,77,78. Out of these, 17 genes viz. Xa579 Xa880,81, Xa1382, Xa1583,84, Xa1985, Xa2086, Xa2487, Xa2588, Xa2689, Xa2889, Xa3190, Xa3267, Xa3391, Xa3492, Xa41(t)73, Xa4293 and Xa44(t)74 are recessive and remaining are dominant (Table 2)88,89. Of the 45 resistance genes Xa194, Xa3/2695,96, Xa597,98, Xa1099, Xa13100, Xa2150, Xa23101, Xa2588 and Xa2778 have been cloned successfully70,78,99-101 and Xa2, Xa4, Xa7, Xa22, Xa30, Xa31 Xa33, Xa34, Xa38, Xa39, Xa40, Xa42 have been fine mapped (Table 2)68,69,72,74,77,102. All these resistance genes follow a Mendelian pattern of gene inheritance and express resistance to a diverse group of Xoo pathogens69,78,89,91,95. The risk of recombination between the molecular marker and the gene of interest has led to a false selection in MAS, whereas it was overcome by the use of functional markers (FMs)103. Functional markers were successfully designed within the coding sequences of different genes for example, pvr1 gene for potyvirus resistance104 in Capsicum sp. and Pm3 gene for powdery mildew resistance in bread wheat105. Cloning some of the identified BB resistance genes Xa1, Xa5, Xa13, Xa21, Xa26 and Xa27 (Table 2)50,78,94,95,97,98,100 made it possible to develop and use FMs106,107. Recently, an FM for Xa21 was developed108 based on the coding sequence of both the alleles (Xa21 and Xa21) reported by Song et al.50. Disease resistance in rice is usually categorized into 2 main groups: qualitative resistance and quantitative resistance. Qualitative resistance is pathogen race-specific and is controlled by a single R gene whose encoded protein can interact directly or indirectly with a corresponding pathogen effector109. It is highly efficient in complete pathogen inhibition and has become favourable to plant breeders due to ease of selection in breeding programme110.

Table 1:Bacterial blight resistance genes identified in wild species of rice
Image for - Impact of Marker Assisted Breeding for Bacterial Blight Resistance in Rice: A Review

Table 2:

List of bacterial blight resistance genes identified in the rice cultivars

Image for - Impact of Marker Assisted Breeding for Bacterial Blight Resistance in Rice: A Review

However, this type of resistance can be easily broken down due to the rapid evolution of pathogen109. This type of resistance has been successfully used for the control of bacterial blight and blast diseases.

Conventional backcross approach: The backcrossing approach was first proposed by Harlan and Pope111 and was practised between the 1930s and 1960s in several crops112. This method is most commonly used to incorporate one or a few traits into an adapted or elite variety113. The other parent, called the ‘donor parent’, possesses one or more genes controlling an important trait which is lacking in the elite variety. In repeated crossings, the hybrids (BC1-n) is backcrossed with the recurrent parent until most of the genes stemming from the donor parent are eliminated except stress resistance114. The expected recurrent parent (RP) genome recovery would be 99.2% by 6 backcrosses, which is most similar to improved variety. The proportion of the RP genome is recovered at a rate of 1(1/2) tC1 for each of the generations of backcrossing115. However, any specific backcross progeny (BC3 or BC2), they will deviate during crossing over resulting in a great chance to get the expected result that is not possible to detect phenotypically. For example, in BC1 population, theoretically, the average percentage of the RP genome is 75% for the entire population. But some individuals possess more or less of the RP genome than others. Those individuals that contain the highest RP genome are selected. But for transferring of quantitative traits, conventional backcross is not an effective method. The presence of undesirable linkages during the backcrossing may prevent the cultivar being improved from promoting the performance of the original recurrent parent. Recessive traits take more time to transfer. Loss of genetic information of recurrent parent may occur in the backcross method.

Marker-assisted selective breeding: MAS can be defined as selection for a trait-based on genotype using associated markers rather than the phenotype of the trait157. This term for the first time was first utilized by Beckmann and Soller158. Since then, accelerated development and availability of molecular markers in plants have made MAS into a major molecular breeding strategy. Molecular marker-assisted selection is recognised to be a highly efficient breeding method because it can offer a rapid and precise selection of the target gene53. The primary considerations of utilizing the DNA markers for MAS is the availability of the tightly linked marker (<5 centiMorgans (cM)), along with the ease of the procedure, cost-effectiveness and highly polymorphic marker system159,160. Marker-assisted backcrossing (MABC) is one of the most anticipated and frequently cited benefits of molecular markers as indirect selection tools in breeding programs161. This approach was first reported for rice by Chen et al.11. They introduced resistance to BB disease into Chinese hybrid parents. It was also described for submergence tolerance using the sub1 gene at International Rice Research Institute (IRRI)162.

The basis of MABC is to transfer one or more desirable genes/QTL from one genetic source (donor parent) into a superior, adapted, elite breeding line (which serves as a recurrent parent) to improve the targeted trait with the help of markers. Unlike traditional backcrossing, marker-assisted backcrossing is based on the marker alleles linked to gene(s)/QTL of interest instead of on phenotypic performance of target trait163. The MABC is accomplished in 3 levels164. In the first level, markers are used for screening the target gene or QTL. This is referred to as ‘foreground selection165,166 although referred to as ‘positive selection’167,168. Marker-assisted foreground selection was proposed by Tanksley169 and investigated in the context of introgression of resistance genes by Melchinger170. The second level of MABC, known as ‘recombinant selection’, involves the selection of backcross progenies having the target gene with tightly linked markers to minimize linkage drag. In conventional backcross breeding, the chromosome segment from donor remains large even after many backcross generations (>10)171,172.

However, the donor chromosome segment (linkage drag) size is significantly reduced173. Recombinant selection is performed usually by using 2 backcross generations160,174 because double recombination events on both sides of target locus are usually rare. The third level of MABC approach involves selecting backcross progenies with the maximum of recurrent parent genomic region by utilizing genome-wide dense molecular markers165,174. This was also referred to as ‘negative selection’ by Takeuchi et al.168. Hence, background selection is very useful in accelerating the recovery of the recurrent parent’s genetic complement, which otherwise takes much longer (6 or more backcross generations) via the conventional backcross method160. In MABC, recurrent parent genome is recovered in BC2 or BC3, BC4 generation165,174-176. The use of background selection during MABC to accelerate the development of an RP with an additional one or more genes has been referred to as ‘variety development or enhancement177 and ‘complete line conversion’178.

Marker-assisted gene pyramiding: The improvement of rice varieties for resistance to the diseases that are prevalent and destructive is necessary for the sustain ability of rice grain yields. Past attempts to achieve varietal resistance to blast and BLB disease have been disappointing, largely due to high levels of variability in the disease populations in growing areas179. For example, a large number of resistance genes for bacterial blight have been identified and tagged from diverse resources by closely linked markers42,70,71,72,120,131. A few of these genes like Xa4 have been incorporated widely in many high yielding varieties through conventional breeding6. However, long term cultivation of varieties with single resistance gene Xa4 has resulted in a significant shift in pathogen-race frequency and consequent breakdown of resistance48. The breeding can provide varieties with blast resistance in rice. In this direction, the pyramiding of multiple disease-resistant genes into a single genetic background can provide durable disease resistance180. The probability of simultaneous pathogen mutations for virulence to defeat two or more effective genes is much lower than with a single gene48.

But, a pyramiding of multiple resistant genes is very difficult through conventional breeding methods due to linkage with some undesirable traits, dominance and epistatic effects of genes governing disease resistance and problems in screening53,181. The advent and easy availability of molecular markers closely associated with each of the resistance genes makes identification of plants with multiple gene possible54. Using the gene pyramiding approach, improved rice cultivars with broad-spectrum durable bacterial blight10,13,15,46,54,182-188, blast resistance genes189, brown plant hopper26,190 resistance genes have been developed by combining different genes. Assembling of more than 2 desirable genes from 2 or more donors into a single genotype or line for a specific trait is referred to as marker-assisted gene pyramiding160.

Marker-assisted breeding for bacterial blight resistance: Marker-assisted backcross breeding (MABB) coupled with phenotypic selection for agronomic, grain and cooking quality traits have been used to incorporate BB resistance genes Xa13 and Xa21 into ‘Pusa Basmati 1’ using IRBB55 (an isogenic line of IR24) as a donor parent. The CAPS marker RG136 linked to Xa13 and STS marker pTA248 linked to Xa21 were used for the foreground selection13. Marker-assisted background analysis integrated with foreground selection was used to identify superior BB resistant lines. One of these lines having maximum genome recovery was released as ‘Improved Pusa Basmati 1’ for commercial cultivation in 2007191 and this is one of the first products of MAS to be used in India. Dokku et al.192,193 pyramided three BB resistant genes (Xa4, Xa5, Xa13 and Xa21)through markers assisted backcross breeding into parental lines Tapaswini and Lalat from IRBB60. The resulting lines ‘Improved Tapaswini and Improved Lalat’ were equivalent to its recurrent parent for yields and grain quality features and possess a high level of resistance to BB.

Similarly, Sundaram et al.15,16 introgressed three BB resistance genesxa5, Xa13 and Xa21into the BB susceptible cultivar Samba Mahsuri and Triguna from a donor line SS1113, lead to the development of IET 19046 as improved samba mahsuri and four elite advanced backcross breeding lines, respectively. These lines have a high yield and broad spectrum of BB resistance. Two traditional basmati varieties namely, Taraori Basmati and Basmati 386 were improved for BB resistance by limited marker-assisted backcrossing coupled with phenotypic selection by transferring Xa21 and Xa13 genes from Improved Samba Mehsuri194.Three BB resistance genes Xa5, Xa13 and Xa21 were introgressed into an indica rice cultivar PR 106 using the marker-assisted selection from a donor line IRBB 62. The pyramided lines with two or three gene combinations exhibited a high level of resistance against different isolates of BB46. Similar selection strategies were used by Salgotra et al.195 for the transfer of three BB resistance genes (Xa5, Xa13 and Xa21) into IRS5441-2, an aromatic breeding line.

Recombinants, IRS 5441-2-21, IRS 5441-2-79 and IRS-2-85 possessed all the three BB resistance genes and fgr (aroma gene) in the homozygous condition and were found to be superior to IRS5441-2 for agronomic performance, grain quality traits and enhanced resistance to BB. Gidamo and Kumaravadivel196 improved CO43 for BB resistance through the introgression of a resistance gene Xa33. Shanti et al.54 introgressed four BB resistance genes Xa4, Xa5, Xa13 and Xa21 into the parental lines of hybrid rice KMR 3, PRR 78, IR58025B, Pusa 6B and Mahsuri. The introgression lines were observed to show very high level of disease resistance against all the ten isolates of Xantomonas. Oryzae pv oryzae. Perumalsamy et al.108 used marker-assisted backcrossing to pyramid three BB resistance (Xa5+Xa13+Xa21) genes into 2 high yielding BLB susceptible indica rice cultivars, ADT43 and ASD16. Out of the 30 pyramided lines, 12 were found significantly superior for grain yield and resistance against BB. Two BB resistance genes (Xa21 and xa13) and a semi-dwarfing gene (sd1) were successfully pyramided in a traditional Basmati Type-3186. To improve BB resistance of 2 varieties Jyothi and IR50, 4 R-genes were introgressed from a donor line based on existing pathogen population184.

Similarly, an elite deepwater cultivar, Jalmagna was improved against BB by introgressing three BB resistance genes (Xa5, Xa13 and Xa21) from Swarna BB pyramid line. Under BB infection, the three genes pyramided lines exhibit a significant yield advantage and high level of resistance to BB over Jalmagna188. Parental lines (Pusa 6B and PRR78) of hybrid PRH 10 was improved by incorporating BB resistance genes Xa13 and Xa21 from Improved Pusa Basmati 1 (Pusa 1460).

Table 3: Commercially released MAS cultivars in Asia
Image for - Impact of Marker Assisted Breeding for Bacterial Blight Resistance in Rice: A Review

Improved lines of Pusa 6B (designated as Pusa 1605) and PRR 78 (designated as Pusa 1601) showed yield advantages of up to 8.24 and 5.23%, respectively. The hybrid combinations generated using improved parental lines showed performance on par with or superior to original PRH 1017,197. Four BB resistance genes (Xa4, Xa5, Xa13 and Xa21) were successfully transferred into 2 parental lines (CRMS 32B and A) of a popular hybrid Rajlaaxmi, in India198. Two BB resistant varieties Angke and Conde were released in 2002, by Department of Agriculture, Indonesia by a combination of phenotypic and marker-aided selection. Angke and Conde carry Xa4 +Xa5 and Xa4+Xa7, respectively199.

Suh et al.187 transferred three BB resistance genes (Xa4+Xa5+Xa21) into an elite japonica rice cultivar Mangeumbyeo using marker-assisted backcrossing (MAB) breeding strategy that led to the development of three elite advanced backcross breeding lines (ABL). The resistant ABL exhibit broad-spectrum resistance against most of the existing B in South Korea without a yield penalty. In China, marker-assisted selection has been successfully employed for the improvement of photosensitive genetic male sterile line 3418200, restorer lines ‘6078’12 Minghui 6311, 4183201 R8006 and R1176202 using the BB resistance gene Xa21 and three popular restorer lines Minghui 63, YR293 and Y1671 using Xa 2361. Three restorer lines (XH2431, 9311 AND WH421) with broad-spectrum and enhanced resistance to BB were developed through marker-assisted breeding and pedigree selection203. Xu et al.204 introgressed two resistance genes against BB into Yihui 1577, an elite restorer line widely used in hybrid rice production in China. The pyramided lines carrying both resistance genes and their derived hybrids showed resistant against all the seven Xoo isolates. The commercially released cultivars of rice with bacterial blight resistance are presented in Table 3. Furthermore, important consideration should be given to determine the stability of bacterial blight resistance genotypes across the various agroclimatic zones especially in the rice-growing belts so that released genotypes can perform better irrespective of the challenge of Genotype×Environment interaction207,208. Similarly, QTL mapping and various other genomic interventions have been successfully implemented in the major cereals like rice and wheat for the improvement of several traits related to biofortification209-211.

CONCLUSION

Bacterial blight is a severe disease of rice and its control using harmful chemicals is not ecofriendly and costly. In contrast, the use of MAS strategies for the control of BB can be vital. MAS has allowed the breeders to recover the favourable alleles at an early stage rather than longer cycles of breeding, thus improving the process of varietal development and ideal parent selection. Molecular marker-based technology is developing and becoming more precise at a rapid rate. The MAS has been well utilized in cereals like and it is very helpful in developing varieties with disease resistance traits. But, the economical and technical considerations are essential for the successful deployment of MAS in a breeding program. Cost reduction is vital to popularize MAS in the breeding programs. The DNA extraction methods that lead to a good quality of DNA needs to be standardized before hand.

Similarly, the challenge imposed by the bacterial blight in rice can be overcome with the help of advanced genomic interventions. This will require detail understanding and implementing the outcomes as soon as possible to delay the losses.

SIGNIFICANCE STATEMENT

In this review, the important information have been compiled regarding the efficacy of molecular breeding in the development of bacterial blight resistance varieties of rice. Disease resistance breeding is a more economical and eco-friendly approach to control the bacterial blight disease of rice. It was hoped that this review will broaden the understanding of the bacterial leaf blight resistance in rice.

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