Screening and Evaluation of Different Wheat Cultivars for Resistance to Sitobion avenae at Seedling and Adult-plant Stages

Xinlun LIU,Changyou WANG,Yajuan WANG,Hong ZHANG,Wanquan JI

State Key Laboratory of Crop Stress Biology for Arid Areas,College of Agronomy,Northwest A&F University,Yangling 712100, China

Screening and Evaluation of Different Wheat Cultivars for Resistance to Sitobion avenae at Seedling and Adult-plant Stages

Xinlun LIU,Changyou WANG,Yajuan WANG,Hong ZHANG,Wanquan JI*

State Key Laboratory of Crop Stress Biology for Arid Areas,College of Agronomy,Northwest A&F University,Yangling 712100, China

In order to clarify the relationships between seedling and adult-plant resistance to English grain aphid Sitobion avenae (Fabricius),94 wheat cultivars were screened and evaluated based on aphid number ratio through artificial inoculation in greenhouse and natural infection in field from 2010 to 2012.The results indicated that 43 wheat cultivars were resistant to aphid at different levels,of which two displayed high resistance,eight moderate resistance and 33 low resistance at adultplant stage.Meanwhile,45 wheat cultivars exhibited aphid resistance at seedling stage,including 5 highly-resistant cultivars,16 moderately-resistant cultivars and 24 low-resistant cultivars.Thirty wheat cultivars showed resistance to aphids to different degrees at both seedling and adult-plant stages,accounting for 31.91%of all tested wheat cultivars,especially that C273 and Lanmai(Shaanxi Zhashui)showed high aphid resistance.Aphid number ratio of wheat cultivars at seedling stage had an extremely significant positive correlation with that at adult-plant stage.Additionally, 66 wheat cultivars exhibited the same resistance to aphids at both seedling and adult-plant stages,accounting for 70.21%of all cultivars.The study demonstrated that inoculation test at seedling stage in greenhouse is a reliable method for identifying wheat resistance to S.avenae.

Sitobion avenae;Wheat;Resistance identification

English grain aphid(Sitobion avenae),a major pest of wheat production all over the world[1-2],seriously affects wheat yield and quality by absorbing plant juice,excreting honeydew,secreting toxin,spreading disease and so on[3-4].Long-term use of insecticide to control aphids not only pollutes environment,but also improves aphid’s drug resistance[5].In recent years,due to different climate conditions and farming systems, wheat ear aphids,especially S.avenae(Fabricius),occurred seriously in the wheat producing regions in Huang-Huai-Hai areas and most northern regions of China,which restricted the output and quality improvement of wheat in China[6-9].A good cultivar with strong resistance to aphids is the most economical and effective way to control wheat aphids. Intercropping of aphid-resistant and conventionalnon-resistant cultivars can significantly reduce aphids at full incidence period and throughout the whole growth period[10-11].It also is beneficial to protect environment and natural enemies,without additional investment and facilities,which conforms to sustainable development.So, screening and application ofnew aphid-resistant wheat gene resources will provide theoretical value and practical significance for the control of aphid pests.

Screening and identifying new aphid-resistant resources play a vital role in the study of aphid resistance of wheat.Many technologies and stan-dards have already been used to screen and identify the aphid resistance of wheat at home and abroad, such as aphid number ratio,aphid index,fuzzy evaluation,aphid life table parameters, electrical penetration graph (EPG)and the loss of 1 000-grain weight[12-17].The aphid number ratio,aphid index and fuzzy evaluation method which are widely used all depend on the ratio of average aphid number per plant(or stem)of one cultivar(or line)to average aphid number per plant(or stem)of all tested cultivars(or lines),but they are different in grading standard of aphid resistance. Field and greenhouse are two main places for conducting test to identify wheat resistance to aphids[12,15,18-19]. The optimum period for identifying aphid resistance is filling stage when aphid infection can cause most loss to wheat.Based on the fact that field tests are easily affected by natural enemies and meteorological factors,field test for one sample should be repeated in 2 years according to “Rules for Resistance Evaluation of Wheat to Diseases and Insect Pests Part 7: Rule forResistance Evaluation of Wheat to Aphids”[20-21],which is timeconsuming.On the contrary,aphid-resistance identification in greenhouse costs much less time and is not affected by phenological factors.In general, a rapid and accurate method for the identification of wheat resistance to aphids is especially important in the breeding of aphid-resistant cultivars.

In this study,seedling resistance in greenhouse and adult-plant resistance in field of tetraploid wheat cultivarsandcommonwheatcultivars were identified based on aphid number ratio with an attempt to screen aphidresistant wheat resources,reveal the correlation of adult-plant resistance and seedling resistance,and to provide theoretical basis for the identification of wheat resistance to aphids.

Materials and Methods

Materials

Among the 94 tested materials provided by the College of Agronomy, Northwest A&F University and Crop Research Institute,Chinese Academy of Agricultural Sciences,one material (Zhong 4 Wumang)was a partial amphiloid of Triticum aestivum-Thinopyrum intermedium;31 materials were tetraploid wheat cultivars, among which one came from Beijing,26 from Shaanxi,and the other four from India, Poland and other countries;62 materials were hexaploid wheat cultivars, among which 37 materials were obtained from Shaanxi,Shanxi,Shandong,Jiangsu and other provinces/ cities,11 materials were local cultivars of Shaanxi, Shanxi, Xinjiang provinces,and 14 materials came from Italy,Australia,Switzerland and Mexico,etc.

Methods

Identification of wheat resistance to aphidDuring 2010-2012,wheat adult-plant resistance to aphid was identified via natural infection in experimental field at the College of Agronomy,Northwest A&F University,Yangling,Shaanxi Province.By referring to“Rules for Resistance Evaluation of Wheat to Diseases and Insect Pests Part 7:Rule for Resistance Evaluation of Wheat to Aphids”,every wheat cultivar was planted in two rows(1 m long each),spacing 0.24 m to each other. Every 10 materials were surrounded by the control cultivar Xiaoyan 6 which was highly susceptible to S.avenae. Under regular field management,one of the three repetitions for theses wheat cultivars was arranged in normal sequence,and the other two repetitions were randomly arranged.To avoid the infection of other wheat aphids,such as greenbug(Schizaphis gramium)and oat birdcherry aphid (Rhopalosiphum padi L.),insect-proof screens were built before grain booting stage[12].Meanwhile,all the tested materials were disinfected to avoid diseases and insect pests.Two weeks later,namely at grain booting stage, the collected naturalpopulation of aphids was inoculated to protecting rows.Aphid number was measured at full incidence period of aphids(wheat milk stage)by referring to the field investigation of aphids proposed by Liu et al.[12].All the results were recorded and analyzed.Wheat seedling resistance to aphids was identified in through artificial inoculation of aphids in greenhouse.In detail,20 seeds of each material were sown in pots,cultivated at 20-22℃and 16 h of supplemental light[220 μmol/(s·m2)]using metal halide lamps every day.Three repetitions were set for each material. Five nymphs were inoculated to every three-leaf seedling of wheat,and then every seedling was covered by a net. The aphid number of every single plant was counted for the first time one week later and once again 3 d later.

Evaluation of aphid resistance

The ratio of the maximum average aphid number per plant of one material among three repetitions to the average aphid number per plant of all materials was calculated to define wheat resistance to aphid.According to Painter’s[22]grading standard,wheat cultivars with the ratio of 0 were immune to aphid;those with the ratio from 0.01 to 0.30 were highly resistant (HR)to aphids;those with the ratio from 0.31 to 0.60 were moderately resistant(MR)to aphids;those with the ratio from 0.61 to 0.90 were lowly resistant(LR)to aphids;those with the ratio from 0.91 to 1.20 were lowly susceptible (LS)to aphids;those with the ratio from1.20 to 1.50 was moderately susceptible(MS)to aphids;and those with the ratio higher than 1.50 was highly susceptible(HS)to aphids.

Data analysis

SPSS16.0 was adopted for variance analysis with one-way ANOVA, multiple comparison with Tukey’s posthoc test and correlation analysis (bivariate correlations).

Results and Analysis

Adult-plant resistance to aphids identified through natural infection in field

As shown in Table 2,all the 94 wheat cultivars were non-immune to aphids,of which 43 cultivars showed resistance at adult-plant stage in all the three years,accounting for 45.74% of all tested materials.Among the 43 aphid-resistant wheat cultivars,only C273 and Lanmai(Zhashui)were highly resistant to aphids,and their aphid number ratios were 0.26 and 0.28 respectively.Eight materials were moderately resistant to aphids,they wereYumai (Xunyang1),Yumai (Xunyang2),Yumai (Xunyang 3), Bailanmai(Xunyang),Yumai(Baihe), Huhanshan (Shanyang),Mazhamai and PI294994,with aphid number ra-tios of 0.40,0.55,0.53,0.50,0.44, 0.60,0.44 and 0.54 respectively.Six foreign materials,Atlas 66,Langdon, PI(high),PI37739,PI262260,RI-107, 18 Shaanxi tetraploid materials including Yumai(Ankang),Lanmai(Shiquan),Laolanmai (Shanyang),etc, eight domestic materials Hongmanghong(Yu 324),Liying 5,Liying 6, Mingxian 169,Nongda 198,Xiaobaidongmai,Shaan 167 and Yanda 1817,and a partialamphidiploid Zhong 4 Wumang exhibited low resistance to aphids.Nineteen materials were low susceptible to aphids,including four tetraploid wheat cultivars,and five foreign hexaploid wheat cultivars. Twenty materials were moderately resistant to aphids,including five tetraploid wheat cultivars(three domestic materials and two foreign materials).Twelve materials showed high Susceptibility to aphids,including two tetraploid cultivars.

Table 1 Information of the wheat cultivars tested in this study

Table 2 Wheat cultivars with stable resistance to S.avenae at adult-plant and seedling stages

Seedling resistance to aphids identified through natural infection in greenhouse

The results showed that 45 materials were resistant to aphids at seedling stage,accounting for 47.87% ofthe 94 cultivars.Among them, C273, PI137739, Yumai(Baihe), Aifanmai (Xixiang) and Lanmai (Zhashui)showed high resistance to aphids 7 and 10 d after artificial inoculation,and their aphid number ratios were 0.29,0.25,0.19,0.17 and 0.13 respectively(Table 2).Sixteen materials showed moderate resistance,including four foreign wheat cultivars (Langdon,Sigeassons,Lovrin 10 and WW),seven Shaanxi local wheat cultivars like Lanmai(Ankang),Lanmai (Shiquan),Yumai(Xunyang 2)and Yumai(Danfeng)and five common cultivars such as Qianjinzao,Shannong NB2(2)-12 and Yanda1817.In addition,24 cultivars showed low re-sistance to aphids,including 6 foreign cultivars (Atlass 66,P720,Lovrin 36, PI262260,PI294994 and RI-15),10 Shaanxi cultivars Lanmai(Ningshaan), Laolanmai(Luonan),Foshoumai(Luonan)and Huhanshan(Shanyang), etc.,8 domestic common cultivars Hongmanghong (Yu 324),Liying 6, Mazhamai,Minxian 169,Shaannong N82(2)-12,Weidong 8,Yan 7578-128 and Xiaobaidongmai. Twenty-two materials were low susceptible to aphids,including one domestic tetraploid wheat cultivar,eight domestic tetraploid wheat cultivars and one foreign common cultivar.Nine materials were moderately susceptible to aphids,of which two materials were tetraploid wheatcultivars.Eighteen cultivars were highly susceptible to aphids,including one foreign tetraploid cultivar and four domestic tetraploid cultivars.

Table 3 The effect of different survey time on the aphid number ratio of wheat cultivars

Table 4 Correlation coefficient of the aphid number ratio of wheat cultivars between adultplant and seedling stages

Comparison ofaphid resistance between seedling stage in the greenhouse and adult plant stage in the field

As could be seen from Table 2,30 cultivars were resistant to aphid at both seedling and adult plant stages, accounting for 31.91%of all tested materials.Among them,C273 and Lanmai(Zhashui)were highly resistant to aphids.Thirty-six cultivars were susceptible to aphids at both seedling and adultplantstages,accounting for 38.30%of the tested materials.Aphidresistant cultivars had significant difference with aphid-susceptible cultivars in aphid numberratio.The seedling resistance and adult-plant resistance of 66 cultivars were basically consistent,accounting for 70.21%of all tested materials.

Multiple comparisons revealed that the aphid number ratio of wheat at seedling stage in greenhouse and adult-plant stage in field was close, with slight difference.No obvious difference of aphid number ratio at different time of seedling stage,or at adult plant stage in different years was observed,indicating that the wheat cultivars had stable resistance to aphids and the experimental results were repeatable(Table 3).

According to correlation analysis, the seedling resistance to aphids in greenhouse shared an extremely significant positive correlation with adultplant resistance in field.The correlation coefficient of aphid number ratio at both stages was 0.359.Hence,we could forecast the aphid resistance at adult-plant stage just depending on that at seedling stage(Table 4).

Discussion

The interaction among plants, diseases and pests is a complexity biological process.The aphid resistance of wheat is determined by genetic characteristics,but also affected by wheat cultivars,growth period,as well as the feed consumption,reproductive capacity,toxicant transmitting ability of aphids and so on.On the basis of“Rules for Resistance Evaluation of Wheat to Diseases and Insect Pests Part 7:Rule for Resistance Evaluation of Wheat to Aphids”(Ministry of Agriculture of the People’s Republic of China)[21],only wheat cultivars with stable aphid resistance can be used as the control;in addition,all the samples should be tested repeatedly for two years,and the result with lower aphid resistance is finally considered if inconsistentresults are obtained in these two years.In the present study, the aphid resistance of 94 wheat materials was detected through artificial inoculation in greenhouse and natural infection in field for three years.As a result,45 and 43 cultivars showed resistance to aphid at seedling and adult-plant stages respectively.While, the majority of aphid-resistant cultivars were tetraploids,or native cultivars with poor agronomic traits,which restricted the extensive use of aphid-resistant gene,but also demonstrated abundant aphid-resistant genes in na-tive cultivars.

Wheat aphid resistance has been identified previously by various methods,such as aphid number ratio[12], aphid index[13],fuzzy evaluation[14], aphid life table parameters[15],electrical penetration graph(EPG)[16],the loss of 1 000-grain weight[17],and all of them have their advantages and disadvantages.This study was conducted to demonstrate whether wheat seedling resistance to aphids was consistent with adult-plant resistance.Duan et al.[23]assessed the seedling and adultplant resistance of 25 wheat cultivars to aphids based on aphid index,and found that their resistance to aphids was basically consistent between seedling and adult-plant stages.The study of Li et al.[24]showed the positive correlation of aphid number between seedling and blooming stages.In this study,aphid number ratio was used as the index to evaluate the resistance of 94 cultivars,and the results revealed that the seedling resistance and adultplant resistance of 66 cultivars were basically consistent,accounting for 70.21%of all tested materials.We also proved that the seedling resistance to aphids in greenhouse shared an extremely significant positive correlation with adult-plant resistance in field, which was consistent with the studies of Duan et al.[23]and Li et al[24].All these results supported that,aphid resistance identification through artificial inoculation at seedling stage in greenhouse was reliable,which not only reduces the effects of climate environment,but also shortens the identification process and saves manpower and physical materials.

We proved that C273 and Lanmai (Shaanxi Zhashui)were highly resistant to aphids,which well agreed with Liu etal.[12].Moreover,PI37739, PI262260,PI294994,Hongmanghong (Yu 324),Liying 6,Xiaobaidongmai, Yanda 1817 and Zhong 4 Wumang were all resistant to aphids at adultplant stage,which was consistent with previous researches[23,25].Poland 305, Linfen 5064,Jinshuang 16,Jimai 26, Shaanyou 225 and Xiaoyan 6 were susceptible to aphids,which well agreed with the studies of Liu et al.[12,23,26-27].However,the identification of some wheat cultivars for aphid resistance showed differentresults with previous studies.For example, our results indicated that Lovrin 10, Jinmai 31,Linyuan 207 and Weidong 8,etc.were susceptible to aphids at adult-plant stage,which was contrary to the results of Li et al[17,23,25-26,28].In addition,Jinmai 31 and Linyuan 207 which breederswere interested in showed different results.According to Painter’s[22]grading standard and aphid number at full aphid incidence period,it was suggested that Jinmai 31 was moderately resistant to aphids in Shanxi in 2007[25],but highly susceptible (with aphid number ratio of 1.65) in Shandong in 2007.However,our studies indicated that it was low susceptible to aphids at adult-plant stage in field,and highly susceptible at seedling stage in greenhouse.In 1989[26]and 2006[23],Linyuan 207 was identified as high-resistance germplasm,but,in 1999,Shi and Zhen’s study indicated that it was low resistant to aphids.In 2011,Qiu et al.[30]regarded it as high-susceptible cultivar.In our study,it was low susceptible to aphids at adult-plant stage in field,moderately susceptible at seedling stage in greenhouse.The different results of resistance identificatioin of one cultivar may be caused by genetic diversity and climate environment[31-32].Zhou et al.[14]investigated the aphid resistance of 200 wheat cultivars in three places of wheat producing areas for two years,ultimately,demonstrated that the aphid resistance varied in different areas or years despite using same material and identification methods.

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Responsible editor:Qingqing YIN

Responsible proofreader:Xiaoyan WU

不同小麦品种资源苗期和成株期麦长管蚜抗性鉴定和分析

刘新伦，王长有，王亚娟，张宏，吉万全*
（西北农林科技大学农学院,旱区作物逆境生物学国家重点实验室,陕西杨凌 712100）

为了明确小麦苗期与成株期麦长管蚜抗性的关系，2010-2012年采用蚜量比值法对94个小麦品种进行了温室苗期人工接种和田间成株期自然感蚜麦长管蚜抗性鉴定。结果表明，43个品种连续3年在成株期对麦长管蚜表现不同程度的抗性，其中高抗品种2个，中抗品种8个，低抗品种33个；45个品种在苗期对麦长管蚜表现不同程度的抗性，其中高抗品种5个，中抗品种16个，低抗品种24个；30个品种在苗期和成株期同时表现抗蚜，占供试品种的31.91%，其中C273和兰麦（陕西柞水）在苗期和成株期均表现为高抗；小麦品种在温室苗期人工接种和田间成株期自然感蚜的蚜量比值呈极显著正相关，苗期和成株期麦长管蚜抗性表现一致的共有66个品种，占供试材料的70.21%。研究表明温室苗期人工接种鉴定小麦麦长管蚜抗性的方法是可靠的，是快速鉴定小麦品种麦长管蚜抗性的有效方法。

麦长管蚜;小麦;抗性鉴定

小麦种质资源发掘与创新利用（2013BAD01B02-6）;国 家自 然 科 学 基 金（30900897);美国唐仲英基金会。

刘新伦（1976-），女，湖南长沙人，博士，助理研究员，从事小麦遗传育种方面研究，E-mail：liuxxlun@126.com。*通讯作者，E-mail：jiwanquan2003@126.com。

2015-06-03

修回日期 2015-07-31

Supported by the Exploration and Innovation and Utilization of Wheat Germplasm Resource (2013BAD01B02-6);the National Natural Science Foundation of China (30900897);the Cyrus Tang Foundation of America.

*Corresponding author.E-mail:jiwanquan2003@126.com

Received:June 3,2015 Accepted:July 31,2015