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Virulence Variations of Puccinia striiformis f. sp. tritici Isolates Collected from Berberis spp. in China

    Affiliations
    Authors and Affiliations
    • Zhiyan Wang
    • Jie Zhao , State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, P. R. China
    • Xianming Chen , United States Department of Agriculture–Agricultural Research Service, Wheat Genetics, Quality, Physiology, and Disease Research Unit and Department of Plant Pathology, Washington State University, Pullman 99164-6430
    • Yuelin Peng , Department of Plant Sciences, Agricultural and Animal Husbandry College of Tibet University, Linzhi, Tibet 86000, P. R. China
    • Jingjing Ji
    • Shilei Zhao
    • Yanjie Lv
    • Lili Huang
    • Zhensheng Kang , State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University
      Published Online:12 Nov 2015https://doi.org/10.1094/PDIS-12-14-1296-RE

      Abstract

      The stripe rust pathogen Puccinia striiformis f. sp. tritici frequently causes significant yield losses in China, due to rapid development of new races that overcome resistance in wheat cultivars. Indirect evidence suggests that sexual reproduction occurs in the P. striiformis f. sp. tritici population in China but direct evidence was still lacking. In this study, a large-scale survey of barberry (Berberis spp.) was conducted in Gansu, Shaanxi, Tibet, and Xinjiang provinces in western China. In total, 9,297 single-aecial (SA) samples were used to inoculate a susceptible wheat cultivar to identify samples of P. striiformis f. sp. tritici. Sixteen of the SA samples were identified as P. striiformis f. sp. tritici. When tested on the wheat differentials for identifying P. striiformis f. sp. tritici races, 15 of the 16 SA samples had different virulence patterns, indicating that they were sexually produced through barberry. From the 16 SA samples, 118 single-uredinium (SU) isolates were obtained, from which 88 virulence patterns were identified when tested on 17 Yr single-gene lines. The virulence patterns had relatively narrow virulence spectra, ranging from 0 to 9, with a mean of four virulences per SU isolates. Of the 17 Yr genes, no virulences were detected for Yr5, Yr10, and Yr15; virulences to YrTr1, Yr24, and Yr27 were extremely low (<3%); those to YrSP, Yr9, Yr28, and Yr2 were low (13.6 to 28.0%); those to Yr7, Yr17, Yr8, and YrExp2 were moderate (33.1 to 48.3%); and those to Yr6, Yr44, and Yr25 were high (52.5 to 72.9%). This study provides direct evidence that natural sexual reproduction occurs in the P. striiformis f. sp. tritici population in China, but the frequency appears to be very low. The sexual reproduction on alternate host plants can generate a great virulence diversity, which may have contributed to the high variation in the P. striiformis f. sp. tritici population in China.

      Stripe rust (yellow rust), caused by the Basidiomycete fungus Puccinia striiformis f. sp. tritici Erikss., is one of the most damaging wheat diseases in the world (Chen 2005; Kang et al. 2010; Rapilly 1979; Wellings 2011). In China, P. striiformis f. sp. tritici has caused several large-scale epidemics resulting in huge yield losses (Li and Zeng 2002). Although fungicides are being used to reduce yield losses, developing resistant cultivars is considered to be the most effective approach for control of the disease (Chen et al. 2014; Wan et al. 2004). However, numerous P. striiformis f. sp. tritici races have been identified, which have overcome resistance in many wheat cultivars that are grown widely (Chen et al. 2009; Hu et al. 2012; Kang et al. 1994, 2010; Li and Zeng 2002; Wan et al. 2003, 2004). It is still a challenge to develop wheat cultivars with long-lasting resistance because new races appear rapidly (Chen et al. 2009; Hu et al. 2012; Kang et al. 2010).

      New races of P. striiformis f. sp. tritici are generated through mutation and somatic recombination, and also possibly through sexual recombination. The stripe rust pathogen accumulates a large number of virulences in single isolates or races through both mutation and clonal production (Chen 2005; Chen et al. 2009; Kang et al. 1994; Line and Qayoum 1992; Wellings and McIntosh 1990). In addition, introduction (natural or human mediated) of new P. striiformis f. sp. tritici races is realized by interregional dissemination through airborne spores or human activities (Chen 2005; Wellings 2011). Based on the heterozygosis of P. striiformis f. sp. tritici, isolates of different races are revealed to combine their virulences to form new races with broad virulence spectra through somatic recombination during the germination and infection processes on or in host tissue (Harder 1984; Kang et al. 1993; Little and Manners 1969; Rodenhiser and Hard-Karrer 1947). A series of previous studies uncovered that the Chinese P. striiformis f. sp. tritici population has a much higher genotypic and virulence diversity than other clonal P. striiformis f. sp. tritici populations (Duan et al. 2010; Lu et al. 2009; Mboup et al. 2009; Shan et al. 1998; Zheng et al. 2013), suggesting sexual reproduction involving the Chinese P. striiformis f. sp. tritici population but lacking direct evidence from alternate hosts. Recently, the sexual recombination of P. striiformis f. sp. tritici was indicated based on the high genetic diversity and recombinant population structure in the Himalayan region of Pakistan, adjacent to the western boundary of China (Ali et al. 2014). Virulence variations are determined not only by the composition of races but also the frequency changes of individual races. Frequency changes can be caused by host selection and genetic drift, and also result from differences of races in fitness and aggressiveness (Chen et al. 2010; Milus et al. 2006; Wan and Chen 2014).

      The discovery of a sexual host for the stripe rust fungus by Jin et al. (2010) demonstrated that the P. striiformis species complex has a sexual cycle. Prior to the discovery, the sexual stage of this rust fungus was thought to be absent (Rapilly 1979; Stubbs 1985). Subsequently, more Berberis spp. (Zhao et al. 2013) and Mahonia spp. (Wang and Chen 2013) were identified as alternate hosts for P. striiformis f. sp. tritici by means of artificial inoculation.

      In China, approximately 250 Berberis spp. have been described (Ying and Chen 2001). Based on our investigations, abundant barberry plants grow wild along mountain slopes and around fields in northwestern and southwestern China (Zhao et al. 2013). Abundant aecia are often found on barberry in these regions and stripe rust is the most common rust disease of wheat; thus, it is likely that P. striiformis f. sp. tritici is cycling through the sexual cycle on barberry. Because the genetic diversity of the P. striiformis f. sp. tritici population in China is high (Kang et al. 1987; Lu et al. 2009; Mboup et al. 2009; Shan et al. 1998; Sharma-Poudyal et al. 2013; Zhan et al. 2012; Zheng et al. 2005, 2013), the fungus is likely to have sexual reproduction. Under controlled conditions, Zhao et al. (2013) demonstrated that P. striiformis f. sp. tritici is able to infect a large number of Berberis spp. They obtained four P. striiformis f. sp. tritici aecial isolates from naturally infected barberry plants in Gansu and Shaanxi provinces. By inoculating the aecial isolates on wheat plants, they identified a large number of races. However, none of them were the same as races that have been identified from wheat fields. The number of aecial isolates was too small to determine how important barberry is for wheat stripe rust epidemics. Thus, a large-scale survey is needed to determine how intensively barberry is infected by the stripe rust fungus under natural conditions in western China.

      The specific objectives of this study were to (i) isolate P. striiformis f. sp. tritici samples from naturally infected barberry plants and (ii) identify virulence characteristics of the P. striiformis f. sp. tritici samples and their single-uredinium (SU) isolates on differentials to determine pathotype and diversity in pathogenicity. The results should provide more insight as to the role of alternate hosts in wheat stripe rust epidemics and generation of diverse races.

      Materials and Methods

      Aecial samples.

      Surveys of rust infection on barberry plants were conducted in Gansu, Shaanxi, Tibet, and Xinjiang provinces in northwestern and southwestern China from April to June 2013. Barberry leaves bearing mature and fresh aecia were collected from bushes of infected Berberis spp. at each of the sampling sites in these provinces, placed in paper bags, and kept in a cool box. After being brought back to the laboratory, the samples were either immediately used to inoculate wheat plants or kept in sealed plastic bags containing desiccant at 4°C for later use.

      Inoculation of wheat plants with aeciospores.

      Wheat ‘Mingxian 169’, susceptible to all Chinese P. striiformis f. sp. tritici races, was grown in plastic pots (7 by 7 by 8 cm) in a rust-free growth chamber set at a temperature of 16 ± 3°C and a photoperiod of 16 h of light and 8 h of darkness. A single aecium (SA) was cut from a barberry leaf using a blade, placed onto a glass slide with two to three drops of deionized water, and crushed gently using an inoculation needle to release aeciospores, forming aeciospore suspensions that were inoculated onto the adaxial surface of primary wheat leaves using a swab. To minimize contamination, the inoculated plants were covered using a transparent plastic cylinder with an open top, and kept for 24 to 36 h at 10°C in darkness in a dew chamber. After incubation, the plants were transferred to a clean growth chamber set to a diurnal cycle of 16°C for the 16-h light period and 13°C for the 8-h dark time. Symptoms and signs were observed and infection types (IT) were recorded based on the 0-to-9 scale for P. striiformis f. sp. tritici (Line and Qayoum 1992) and the 0-to-4 scale for P. graminis f. sp. tritici (Stakman et al. 1962) 15 to 20 days after inoculation. Urediniospores were collected from wheat leaves inoculated with aeciospores from each aecium and treated as an SA sample.

      Establishment of SU population.

      The wheat leaves inoculated with aeciospores were kept for 5 to 8 days for collecting urediniospores to represent the SA samples. For each SA sample, 10 to 14 fresh uredinia were randomly picked from wheat leaves inoculated with aeciospores using a metal office pin tipped with a small amount of Vaseline jelly to inoculate new wheat leaves for establishing an SU isolate population. To ensure that urediniospores were from an SU, uredinia that were not completely erupted through the host tissue were used. The resultant urediniospores were used to inoculate new Mingxian 169 seedlings with a fine brush with deionized water for increasing spores. The inoculated wheat plants were kept in a dew chamber at 10°C for 24 h, and grown in a growth chamber at 13 to 16°C, with a photoperiod of 16 h of light and 8 h of darkness. If the amount of urediniospores was not enough, urediniospore multiplication was repeated following the method mentioned above.

      Determination of virulence phenotypes of P. striiformis f. sp. tritici isolates.

      The virulence patterns of the SA samples were determined by inoculating fresh urediniospores onto seedlings of the set of 19 wheat genotypes used to differentiate Chinese P. striiformis f. sp. tritici races, according to the method described by Chen et al. (2009). Similarly, the virulence patterns of the SA and SU isolates were determined on 17 Yr single-gene lines, most of which have been used to differentiate races in the United States and other countries (Sharma-Poudyal et al. 2013; Wan and Chen 2014). The procedures and conditions for inoculation and growing inoculated plants were the same as described above. The IT data were recorded using the 0-to-9 scale for P. striiformis f. sp. tritici and 0-to-4 scale for P. graminis f. sp. tritici as described above.

      Results

      SA samples of P. striiformis f. sp. tritici from barberry plants.

      Six Berberis spp. were surveyed at 26 sites located in four provinces in this study. In total, 9,297 single aecia were collected from 151 bushes and tested on susceptible Mingxian 169 wheat (Table 1). Of the collected aecial samples, 16 aecia produced typical P. striiformis f. sp. tritici uredinia with high IT, resulting in 16 SA samples, designated as U1 to U16. The 16 SA samples were obtained from three Berberis spp.: Berberis aggregata in Gansu, B. polyantha in Tibet, and B. shensiana in Shaanxi. No P. striiformis f. sp. tritici isolates were obtained from aecial samples from Xinjiang. This indicated that P. striiformis f. sp. tritici was collected at a low overall frequency of 0.17%. Most of the aecial samples inoculated on Mingxian 169 produced necrotic flecks without uredinia (IT 1 to 2 using the 0-to-9 scale for P. striiformis f. sp. tritici or IT 0; using the 0-to-4 scale for P. graminis f. sp. tritici) or no symptom (IT 0) (Table 2). The species of these aecia could not be determined in the present study. Simultaneously, 14 P. graminis f. sp. tritici samples were obtained, also at a low frequency (0.13%), from the tested SA samples.

      Table 1. Number of samples of Puccinia striiformis f. sp. tritici and P. graminis f. sp. tritici recovered from aecia on Berberis spp. collected from Gansu, Shaanxi, Tibet, and Xinjiang provinces in 2013

      Table 2. Identification of Puccinia striiformis f. sp. tritici and P. graminis f. sp. tritici aecial samples recovered by inoculation of Mingxian 169 wheat with aeciospores of single aecium collected from naturally infected barberry plants in 2013

      Virulence patterns of the P. striiformis f. sp. tritici SA samples.

      The 16 P. striiformis f. sp. tritici SA samples had 15 different virulence patterns on the Chinese differential genotypes (Table 3). Compared with the 67 P. striiformis f. sp. tritici races from wheat as reported by Zhan et al. (2012), 14 of the patterns were different from those of the previously reported races. The two isolates (U2 and U3) collected from B. aggregata in Gansu had a virulence pattern similar to CYR32, a predominant P. striiformis f. sp. tritici race in the region. In addition, SA isolate U10 from B. shensiana in Shaanxi had a virulence pattern similar to that of CYR32, with the only difference in its avirulence on wheat differential Danish 1. Isolates U5 and U7, also from B. shensiana in Shaanxi, had virulence patterns similar to CYR20, with additional virulences on differentials Virgilio and Suwon 11 in both U5 and U7 and additional virulence on differential Jubilejina 2 in U5. Isolate U4 from B. polyantha in Tibet had the same virulence pattern as CYR20, except for its virulence on differentials Fengchan 3 and Suwon 11. None of the SA samples were virulent to Zhong 4 (Yr gene unknown), Triticum spelta ablum (Yr5), and Guinong 22 (Yr26), similar to the P. striiformis f. sp. tritici populations from wheat crops.

      Table 3. Avirulence and virulence patterns of 16 Puccinia striiformis f. sp. tritici samples obtained from 16 single aecium produced on naturally infected Berberis spp. on the set of 19 wheat cultivars used to differentiated P. striiformis f. sp. tritici races

      The 16 P. striiformis f. sp. tritici SA samples were also tested on the 17 Yr single-gene lines (Table 4). Isolates U2 and U3 produced the same virulence patterns as race CYR32 on the Yr single-gene lines (data not shown). None of the 16 SA samples produced identical virulence patterns, similar to the results obtained with the Chinese differentials.

      Table 4. Avirulence and virulence patterns of 16 Puccinia striiformis f. sp. tritici samples obtained from 16 single aecium on wheat Yr single gene lines

      Most of the SA samples had mixed IT on some of the differential genotypes and all of the SA samples had mixed IT on many Yr single-gene lines, indicating that the SA samples comprised isolates with different virulence patterns. Therefore, SU isolates were established from each of the SA samples and tested on the 17 Yr single-gene lines.

      Virulence patterns of SU isolates.

      From the 16 SA samples, 118 SU isolates were obtained. The SU isolates were identified to have 88 virulence patterns based on the IT data of the 17 Yr single-gene lines (Table 5). The high pattern/isolate ratio (1:1.3) clearly show that these isolates were produced through sexual reproduction.

      Table 5. Avirulence and virulence patterns of 118 single uredinial isolates of Puccinia striiformis f. sp. tritici obtained from 16 single-aecium samples collected from naturally infected Berberis spp.

      The 88 virulence patterns had relatively narrow virulence spectra, ranging from 0 to 9 with a mean of 4 virulences (Table 5) compared with their SA samples (Table 4). The frequencies of the virulences to the 17 Yr genes among the 118 SU isolates are shown at the bottom of Table 5. No virulences were detected for Yr5, Yr10, and Yr15; virulences to YrTr1, Yr24, and Yr27 were extremely low (<3%); those to YrSP, Yr9, Yr28, and Yr2 were low (13.6 to 28.0%); those to Yr7, Yr17, Yr8, and YrExp2 were moderate (33.1 to 48.3%); and those to Yr6, Yr44, and Yr25 were high (52.5 to 72.9%).

      Most of the virulence patterns were represented by only one isolate, while only 15 (17%) patterns had two or more isolates (Table 5). Nine virulence patterns (VP-1, VP-6, VP-39, VP-41, VP-44, VP-46, VP-61, VP-69, and VP-77) each had two isolates, two patterns (VP-13 and VP-70) each had three isolates, two patterns (VP-2 and VP-65) each had four isolates, one pattern (VP-23) had six isolates, and one pattern (VP-7) had eight isolates. Isolates with an identical virulence pattern were generally from different SA samples. Some of the pattern-shared isolates were from different Berberis spp. and different provinces. For example, VP-7 consisted of five SU isolates (U1-7, U1-10, U2-1, U2-10, and U6-1) from B. aggregata in Gansu and three isolates (U5-1, U9-3, and U10-6) from B. shensiana in Shaanxi.

      Discussion

      In this study, 9,297 aecia were individually tested on Mingxian 169 wheat, from which 16 P. striiformis f. sp. tritici SA samples were obtained. These isolates and their derived 118 SU isolates were clearly shown by virulence tests to be produced from sexual reproduction on barberry plants. This study, together with a previous study (Zhao et al. 2013), provided direct evidence that P. striiformis f. sp. tritici sexual reproduction exists in China, as was previously speculated based on marker analysis of the P. striiformis f. sp. tritici population from wheat fields (Mboup et al. 2009). Compared with the previous study reporting only four isolates from Gansu and Shaanxi (Zhao et al. 2013), the present study has extended the geographic areas where P. striiformis f. sp. tritici sexual reproduction occurs from the northwest to southwest of China.

      Many regions in western China, especially southern Gansu and northwestern Sichuan, are regarded as hotspots for wheat stripe rust in China according to the history of the disease epidemics (Li and Zeng 2002). In these regions, P. striiformis f. sp. tritici oversummers or overwinters in the uredinial stage and provides inoculum to initiate infection on wheat within and among the regions and further spread to regions in eastern China (Chen et al. 2009; Shan et al. 1998). More importantly, most of the P. striiformis f. sp. tritici races (approximately 90%), particularly those that have overcome resistance in major wheat cultivars, were identified first in the hotspot regions (Chen et al. 2009; Huang et al. 2014; Kang and Li 1984; Kang et al. 1987, 1994; Liu et al. 2010; Wang et al. 1986). Based on our previous surveys, there are abundant barberry plants with rust fungal aecia adjacent to wheat fields in Gansu and Shaanxi provinces but only four P. striiformis f. sp. tritici samples were isolated (Zhao et al. 2013). The present study expanded our knowledge of rusting barberry plants existing in Tibet and Xinjiang. Interestingly, we isolated P. striiformis f. sp. tritici from the aecial samples collected from Tibet but not from those of Xinjiang. Thus, the barberry bushes adjacent to wheat fields may provide great opportunities for the spread of basidiospores from wheat straws to infect barberry and aeciospores from barberry to infect wheat. However, whether barberry plants provide aeciospores to initiate stripe rust in wheat fields needs further study because stripe rust was generally observed in wheat fields when we saw aecia on barberry plants.

      In the present study, only 16 of 9,297 aecia were clearly identified as P. striiformis f. sp. tritici, indicating a very low frequency (0.17%). Stripe rust is the most frequent disease of wheat in the surveyed regions. The low frequency of P. striiformis f. sp. tritici on barberry plants may suggest really low infection by the pathogen under natural conditions. The direct connection between the stem rust fungi on alternate hosts and cereal crops have been well known for centuries (Roelfs 1982; Zadoks and Bouwman 1985). However, no such phenomenon has been reported for stripe rust. The low infection frequency may explain why apparent connections between stripe rust of wheat and barberry have not been observed. The low level of P. striiformis f. sp. tritici infection on barberry could be due to a low survival rate of teliospores after winter. Further studies are needed to test this hypothesis.

      More than 99% of the individual aecia were not identified as either P. striiformis f. sp. tritici or P. graminis f. sp. tritici because they did not produce uredinia on the inoculated wheat plants. In addition to P. striiformis and P. graminis, many other Puccinia spp. are able to infect barberry plants. These species include P. brachypodii (Payak 1965); P. poa-nemoralis, P. pygmaea, P. montanensis, and P. brachypodii-phoenicoidis (Cummins and Greene 1966); P. arrhenatheri (Naef et al. 2002); and P. striiformis f. sp. poae (Jin et al. 2010). Therefore, most aecial pustules observed on barberry plants might be other Puccinia spp. or formae speciales of P. striiformis and P. graminis. Further studies are needed to identify rust fungal species and their frequencies on barberry plants. We are currently developing molecular markers and using sequencing techniques to study the different Puccinia spp. on barberry. In addition, some of the aecial inoculations might not have been successful, due to possible reduction of the viability of aecia during the travel and storage before inoculation. Some aecia might be P. striiformis f. sp. tritici but avirulent on Mingxian 169. To further improve the inoculation and identification efficiencies, either wheat genotypes universally susceptible to P. striiformis f. sp. tritici and P. graminis f. sp. tritici or different genotypes susceptible to different rust fungi should be used in tests with split aecial samples. Together with suitable molecular markers and sequencing, accurate frequencies of various Puccinia spp. on barberry should be determined.

      Two of the SA samples had an overall virulence pattern similar to the predominant P. striiformis f. sp. tritici race CYR32 in the region (Chen et al. 2009; Wan et al. 2004; Zhan et al. 2012). This result more likely indicated that the sources of inoculum (teliospores on wheat straw) for infection of the barberry plants were from the P. striiformis f. sp. tritici population in the nearby wheat fields. Most virulence patterns identified from the 118 SU isolates have not been found in wheat isolates. This could be due to stripe rust resistance conferred by various resistance genes in wheat cultivars. Because most isolates had relatively narrow virulence spectra, they were unable to infect commercially grown wheat cultivars. For example, a large number of wheat cultivars have resistance gene Yr9 (Zeng et al. 2014), and this gene alone can prevent infection by 80% of the SU isolates. Yr24 (= Yr26) is in many of the wheat cultivars developed in the recent years (Zeng et al. 2014), and cultivars with that gene can prevent infection of 97.5% of the SU isolates detected in the present study. The present study shows that Yr5, Yr10, and Yr15 are still resistant against all virulent patterns identified from the sexual population, as well as against the predominant races such as CYR32 in the asexual population. However, further studies should be conducted to determine virulence exchanges between the sexual population and asexual population.

      Although P. striiformis f. sp. tritici on barberry plants may not play a major role in initiating stripe rust on wheat crops, it may generate new and unique races which could damage wheat crops, even at a low frequency. To reduce the potential of new races damaging wheat crops, race-nonspecific resistance or diverse resistance genes should be used to develop wheat cultivars with stripe rust resistance, no matter whether or not P. striiformis f. sp. tritici infecting barberry plants can provide initial inoculum to infect wheat crops or generate new races attacking specific wheat cultivars.

      Acknowledgments

      This study was supported by National Key Basic Research Program of China (2013CB127700), International Science & Technology Cooperation Program of China (2011DFG32990), the earmarked fund for Modern Agro-industry Technology Research System Project in China (CARS-3-1-11), National Natural Science Foundation of China (31271986), the 111 Project from the Ministry of Education of China (B07049), and Program for New Century Excellent Talents in University.

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      Z. Wang and J. Zhao contributed equally to this work.