对荻草谷网蚜具有抗生特性的春小麦品种筛选与鉴定

doi:10.1016/S2095-3119(21)63716-4

摘要/Abstract

摘要：

本研究首先通过室内生物测定，对114个埃塞俄比亚春小麦品种（系）和22个中国春小麦品种（系）进行了对麦蚜优势种荻草谷网蚜（Sitobion miscanthi）抗生性筛选及鉴定，并利用刺吸电位图谱技术（EPG）和高效液相色谱（HPLC）分别对抗蚜小麦品种上蚜虫取食行为、酚类物质含量进行检测与分析。结果表明，供试小麦品种中，对荻草谷网蚜表现抗性的品种（系）共64个，其中高抗2个，中抗27个、低抗35个。与感蚜品种北京837相比，荻草谷网蚜在轮选145，Wane，轮选6，轮选103及5215等抗蚜品种（系）上，其成蚜前期及生殖前期显著延长，生殖历期缩短，繁殖力、内禀增长率（r_m）与周限增长率（λ）显著下降；EPG结果表明，在抗蚜品种（系）上蚜虫取食行为受到显著影响，蚜虫口针穿刺历期及唾液分泌历期显著增加，而在韧皮部取食历期显著缩短，表明抗蚜性可能发生在韧皮部取食阶段，并与蚜虫口针穿刺叶肉细胞困难有关。酚类物质含量测定结果表明，与感蚜品种北京837相比，轮选145，轮选103与轮选6叶片中阿魏酸含量较高；轮选145中p-香豆酸含量较高；轮选145，Wane及轮选6中香草酸含量较高；轮选103与5215分别含有较高的紫丁香酸与咖啡酸含量。相关性分析表明，小麦叶片中的一些酚类物质含量如香草酸与香豆酸与蚜虫发育历期呈显著正相关，而与蚜虫繁殖力呈负相关。因此，推测酚类物质含量是小麦对荻草谷网蚜产生抗生性的主要原因。本研究鉴定的抗蚜春小麦品种（系）将有助于春小麦抗蚜品种的培育及利用。

Abstract:

Resistant cultivar deployment is an effective method for cereal aphid management. Under greenhouse conditions, preliminary antibiosis resistance screening was conducted on 114 Ethiopian and 22 Chinese spring wheat accessions. After performing a bioassay to determine antibiosis resistance, aphid feeding behaviour and phenolic acid content analyses were performed on the aphid resistant wheat accessions by electrical penetration graph (EPG) and high performance liquid chromatography (HPLC), respectively. Among the wheat accessions, two high resistances, 27 moderate-resistances, and 35 low-resistances to Sitobion miscanthi were identified. The antibiosis resistance test showed prolonged pre-adult and pre-reproductive periods, shorter reproductive periods, lower fecundity, an intrinsic rate (r_m) of increase, and a finite rate (λ) of increase of S. miscanthi on Lunxuan 145, Wane, Lunxuan 6, 204511, Lunxuan 103 and 5215 than those on the aphid-susceptible accession Beijing 837. The changes for the parameters of aphid feeding behaviour, including spending a longer time in the penetration and phloem salivation phases and less time in the phloem sap-feeding phase on the resistant wheat accessions, the aphid resistance may occur during the phloem phase and may be due to mechanicalAdditionally, the HPLC analysis showed higher contents of: 1) ferulic acid in Lunxuan 145, Lunxuan 103 and Lunxuan 6; 2) p-coumaric acid in Lunxuan145; 3) vanillic acid in Lunxuan 145, Wane and Lunxuan 6; 4) syringic acid in Lunxuan 103; and 5) caffeic acid in 5215. The contents of some phenolic acids within wheat leaves, such as p-courmaric acid and vanillic acid showed significant positive correlation with the duration of aphid development, but negative correlation with the aphid fecundity. The concentrations of these acids may be the causes of antibiosis resistance to S. miscanthi. The identification of grain aphid-resistant wheat accessions in our study will be helpful in future breeding program for pest control.

Key words: Sitobion miscanthi , spring wheat accessions , antibiosis resistance , electronic penetration graph , high-performance liquid chromatography , phenolic acid concentrations

. 对荻草谷网蚜具有抗生特性的春小麦品种筛选与鉴定[J]. Journal of Integrative Agriculture, 2022, 21(8): 2329-2344.

Kifle Gebreegziabiher GEBRETSADIK, ZHANG Yong, CHEN Ju-lian. Screening and evaluation for antibiosis resistance of the spring wheat accessions to the grain aphid, Sitobion miscanthi (Takahashi) (Hemiptera: Aphididae)[J]. Journal of Integrative Agriculture, 2022, 21(8): 2329-2344.

参考文献

Ahmed E, Arshad M, Khan M Z, Amjad M S, Sadaf H M, Riaz I, Ahmad N. 2017. Secondary metabolites and their multidimensional prospective in plant life. Journal of Pharmacognosy and Phytochemistry, 6, 205–214.
Akköprü E P, Atlihan R, Okut H, Chi H. Demographic assessment of plant cultivar resistance to insect pests: a case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars, Journal of Economic Entomology, 108, 378–387.
Alkhedir H, Karlovsky P, Vidal S. 2013. Relationship between water soluble carbohydrate content, aphid endosymbionts and clonal performance of Sitobion avenae on cocksfoot cultivars. PLoS ONE, 8, e54327.
Anaii M M, Yali M P. 2018. Resistance of nine wheat cultivars and lines to green bug, Schizaphis graminum (Rondani) in Iran. Journal of Agricultural Science and Technology, 20, 1173–1185.
Annan I B, Tingey W M, Schaefers G A, Tjallingii W F, Backus E A, Saxena K N. 2000. Stylet penetration activities by aphis craccivora (Homoptera: Aphididae) on plants and excised plant parts of resistant and susceptible cultivars of cowpea (Leguminosae). Annual of the Entomological Society of America, 93, 133–140.
Anteneh A, Asrat D. 2020. Wheat production and marketing in Ethiopia: Review study. Cogent Food & Agriculture, 6, 1–14.
Aradottir G I, Martin J L, Clark S J, Pickett J A, Smart L E. 2017. Searching for wheat resistance to aphids and wheat bulb fly in the historical Watkins and Gediflux wheat collections. Annals of Applied Biology, 170, 179–188.
Awmack C S, Leather S R. 2002. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817–844.
Baradevanal G. 2013. Antibiosis effect of phenolic acid (ferulic acid and p-coumaric acid) on maize spotted stem borer, Chilo partellus (Swinehoe) (Lepidoptera: Pyralidae). Indian Journal of Entomology, 75, 248–250.
van Bel A J E, Will T. 2016. Functional evaluation of proteins in watery and gel saliva of aphids. Frontiers in Plant Science, 7, 1840.
Botha A M, van Eck L, Burger N F V, Swanevelder Z H. 2014. Near-isogenic lines of Triticum aestivum with distinct modes of resistance exhibit dissimilar transcriptional regulation during Diuraphis noxia feeding. Biology Open, 3, 1116–1126.
Boz H. 2015. Ferulic acid in cereals - A review. Czech Journal of Food Sciences, 33, 1–7.
Cao H H, Pan M Z, Liu H R, Wang S H, Liu T X. 2015. Antibiosis and tolerance but not antixenosis to the grain aphid, Sitobion avenae (Hemiptera: Aphididae), are essential mechanisms of resistance in a wheat cultivar. Bulletin of Entomological Research, 105, 448–455.
Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Chen Y H, Gols R, Stratton C A, Brevik K A, Benrey B. 2015. Complex tritrophic interactions in response to crop domestication: predictions from the wild. Entomologia Experimentalis et Applicata, 157, 40–59.
Chi H. 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17, 26–34.
Chi H, Liu H. 1985. Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology Academia Sinica, 24, 225–240.
Chrzanowski G, Leszczyński B, Czerniewicz P, Sytykiewicz H, Matok H, Krzyzanowski R, Sempruch C. 2012. Effect of phenolic acids from black currant, sour cherry and walnut on grain aphid (Sitobion avenae F.) development. Crop Protection, 35, 71–77.
Courtois E A, Baraloto C, Paine C T, Petronelli P, Blandinieres P A, Stien D, Chave J. 2012. Differences in volatile terpene composition between the bark and leaves of tropical tree species. Phytochemistry, 82, 81–88.
Deloach C J. 1974. Rate of increase of populations of cabbage, green peach, and turnip aphids at constant temperatures. Annuals of the Entomological Socialy of America, 67, 332–340.
Doryanizadeh N, Moharramipour S, Hosseininaveh V, Mehrabadi M. 2016. Effect of eight Cucumis genotypes on life table and population growth parameters of melon aphid: An approach to assess antibiosis resistance. Journal of Agriculture, Science and Technology, 18, 1819–1832.
Eddoha R, Lhaloui S, Elabbyui M, Nasser B, Essamadi A. 2014. Peroxidase activity and phenolic content in barley and wheat infested by cecidomyiid insects. International Journal of Scientific and Engineering Research, 5, 46–53.
Eleftherianos I, Vamvatsikos P, Ward D, Gravanis F. 2006. Changes in the levels of plant total phenols and free amino acids induced by two cereal aphids and effects on aphid fecundity. Journal of Applied Entomology, 130, 15–19.
Filho J E G, Padua L E D M, Portela G L F, Sousa F D M. 2019. Thermal requirements and age-specific life tables of cowpea aphids in cowpea under natural field conditions. Arquivos do Instituto Biológico, 86, e0502018.
Furch A C U, van Bel A J E, Will T. 2015. Aphid salivary proteases are capable of degrading sieve-tube proteins. Journal of Experimental Botany, 66, 533–539.
Gantner M, Agnieszka N, Piesik D. 2019. Effect of phenolic acid content on acceptancof hazel cultivars by filbert aphid. Plant Protection Science, 55, 116–122.
Giordanengo P. 2014. EPG-Calc: A PHP-based script to calculate electrical penetration graph (EPG) parameters. Arthropod–Plant Interactions, 8, 163–169.
Golan K, Sempruch C, Gorska E, Czerniewicz P, Lagowska B, Kot I, Kmiec K, Magierowicz K, Leszczynski B. 2017. Accumulation of amino acids and phenolic compounds in biochemical plant responses to feeding of two different herbivorous arthropod pests. Arthropod-Plant Interactions, 11, 675–682.
Goławska S. 2010. Effect of various host-plants on the population growth and development of the pea aphid. Journal of Plant Protection Research, 50, 225–228.
Goodman D. 1982. Optimal life histories, optimal notation, and the value of reproductive value. The American Naturalist, 119, 803–823.
Guerrieri E, Digilio M C. 2008. Aphid-plant interactions: A review. Journal of Plant Interactions, 3, 223–232.
Hatfield J L, Beres B L. 2019. Yield gaps in wheat: path to enhancing productivity. Frontiers in Plant Science, 10, 1603.
Hu X S, Zhao H Y, Hu Z Q, Li D H, Zhang Y H. 2008. EPG comparison of Sitobion avenae (Fab.) feeding behavior on three wheat varieties. Agricultural Sciences in China, 7, 180–186.
Huang Y, Chi H. 2012. Assessing the application of the jackknife and bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive. Journal of Agriculture and Forestry, 61, 37–45.
Jaouannet M, Rodriguez P A, Thorpe P, Lenoir G C J, MacLeod R, Escudero-Martinez C, Bos J I. 2014. Plant immunity in plant–aphid interactions. Frontiers in Plant Science, 5, 663.
Jiang X, Zhang Q, Qin Y G, Yin H, Zhang S Y, Li Q, Zhang Y, Fan J, Chen J L. 2019. A chromosome-level draft genome of the grain aphid Sitobion miscanthi. GigaScience, 8, giz101.
Jin M, Han B Y. 2007. Probing behavior of the tea green leafhopper on different tea plant cultivars. Acta Ecologica Sinica, 27, 3973–3982. (in Chinese)
Junaid K, Khan S A, Khan I, Rizwan S, Shah A, Khan Z. 2016. Study on different components of resistance in wheat genotypes to green bug (Schizaphis graminum) (Rondani). Pakistan Journal of Zoology, 48, 981–987.
Kandil A, Li J, Vasanthan T, Bressler D C. 2012. Phenolic acids in some cereal grains and their inhibitory effect on starch liquefaction and saccharification. Journal of Agricultural and Food Chemistry, 60, 8444–8449.
Kim K, Tsao R, Yang R, Cui S W. 2006. Food chemistry phenolic acid profiles and antioxidant activities of wheat bran extracts and the effect of hydrolysis conditions. Food Chemistry, 95, 466–473.
Leszczynski B, Tjallingii W E, Dixon A F G, Swiderski R. 1995. Effect of methoxyphenols on grain aphid feeding behaviour. Entomologia Experimentalis et Applicata, 75, 157–162.
Leszczynski B, Warchol J, Niraz S. 1985. The influence of phenolic compounds on the preference of winter wheat cultivars by cereal aphids. International Journal of Tropical Insect Science, 6, 157–158.
Levakova L, Lacko-Bartosova M. 2017. Phenolic acids and antioxidant activity of wheat species: A review. Agriculture, 63, 92–101.
Li F Q, Kong L R, Liu Y S, Wang H Z, Chen L, Peng J H. 2013. Response of wheat germplasm to infestation of English grain aphid (Hemiptera: Aphididae). Journal of Economic Entomology, 106, 1473–1478.
Li H J, Zhou Y, Xin W L, Wei Y Q, Zhang J L, Guo L L. 2019. Wheat breeding in northern China: Achievements and technical advances. Crop Journal, 7, 718–729.
Li S J, Zhang Z Y, Wang X Y, Ding H J, Ni H X, Sun J R, Chen J L. 1998. Study on identification of aphid resistance of wheat varieties (lines) by fuzzy recognition technology. Plant Protection, 5, 15–16. (in Chinese)
Li X G, Zhang T L, Wang X X, Hua K, Zhao L, Han Z M. 2013. The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. International Journal of Biological Sciences, 9, 164–173.
Liu F H, Kang Z W, Tan X L, Fan Y L, Tian H G, Liu T X. 2020. Physiology and defense responses of wheat to the infestation of different cereal aphids. Journal of Integrative Agriculture, 19, 1464–1474.
Loxdale H D, Balog A. 2018. Aphid specialism as an example of ecological-evolutionary divergence. Biological Reviews, 44, 642–657.
Lu Y H, He Y P, Gao X W. 2013. Comparative studies on acetylcholinesterase characteristics between the aphids, Sitobion avenae and Rhopalosiphum padi. Journal of Insect Science, 13, 9.
Marimuthu M, Smith C. 2012. Barley tolerance of Russian wheat aphid (Hemiptera: Aphididae) biotype 2 herbivory involves expression of defense response and developmental genes. Plant Signaling and Behavior, 7, 337–341.
Medina-Ortega K J, Walker G P. 2015. Faba bean forisomes can function in defence against generalist aphids. Plant, Cell and Environment, 38, 1167–1177.
Miller H R, Randolph T L, Peairs F B. 2003. Categories of resistance at four growth stages in three wheats resistant to the Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology, 96, 673–679.
Moctezuma C, Hammerbacher A, Heil M, Gershenzon J, Mendez-Alonzo R, Oyama K. 2014. Specific polyphenols and tannins are associated with defence against insect herbivores in the tropical oak Quercus oleoides. Journal of Chemical Ecology, 40, 458–467.
Moreno-Delafuente A, Garzo E, Moreno A, Fereres A. 2013. A plant virus manipulates the behavior of its whitefly vector to enhance its iransmission efficiency and spread. PLoS ONE, 8, e61543.
Painter R. 1951. Insect resistance in crop plants. Journal of Soil Science, 72, 481.
Pavela R. 2007. The feeding effect of polyphenolic compounds on the Colorado potato beetle [Leptinotarsa decemlineata (Say)]. Test Technology, 1, 81–84.
Pawel C, Grzegorz C, Hubert S, Iwona S, Bogumil L. 2016. Aphidicidal and deterrent activity of phenolic acid extracts from some herbal plants towards Myzus persicae Sulz. and Rhopalosiphum padi. Fresenius Environmental Bulletin, 25, 5714–5721.
Peterson R K, Varella A C, Higley L G. 2017. Tolerance: the forgotten child of plant resistance. PeerJ, 5, e3934.
Razmjou J, Ramazani S, Naseri B, Ganbalani G N, Dastjerdi H R. 2011. Resistance and susceptibility of various wheat varieties to Sitobion avenae (Hemiptera: Aphididae) in Iran. Applied Entomology and Zoology, 46, 455–461.
Sandanayaka M, Charles J G. 2017. Potential use of electrical penetration graph (EPG) technology for biosecurity incursion response decision making. New Zealand Plant Protection, 70, 1–15.
Santiago R, Malvar R A, Baamonde M D, Revilla P. 2005. Free phenols in maize pith and their relationship with resistance to Sesamia nonagrioides (Lepidoptera: Noctuidae) attack. Journal of Economic Entomology, 98, 1349–1356.
Sarria E, Cid M, Garzo E, Fereres A. 2009. Excel workbook for automatic parameter calculation of EPG data. Computers and Electronics in Agriculture, 67, 35–42.
SAS (Statistical Analysis System). 1999. SAS/STAT/User’s guide. Version 8. SAS Institute Inc., Cary, NC.
Seo B Y, Kim E Y, Ahn J J, Kim Y, Kang S. 2020. Development, reproduction, and life table parameters of the foxglove aphid, Aulacorthum solani Kaltenbach (Hemiptera: Aphididae), on soybean at constant temperatures. Inscets, 26, 296.
Shewry P R. 2009. Wheat. Journal of Experimental Botany, 60, 1537–1553.
Silva A M, Sampaio M V, de Oliveira R S, Korndorfer A P, Ferreira S E, Polastro G C, Dias P A S. 2013. Antibiosis and non-preference of Sitobion avenae (F.) (Hemiptera: Aphididae) on leaves and ears of commercial cultivars of wheat (Triticum aestivum). Neotropical Entomology, 42, 304–310.
Su Q, Zhou Z X, Zhang J M, Shi C H, Zhang G H, Jin Z Y, Wang W K, Li C R. 2017. Effect of plant secondary metabolites on common cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Entomological Research, 48, 18–26.
Taheri S, Raznaou J, Rastegari N. 2010. Fecundity and development rate of the bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hom.: Aphididae) on six wheat cultivars. Plant Protection Science, 46, 72–78.
Tjallingii W F. 2006. Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany, 57, 739–745.
Urbanska A, Tjallingii W F, Dixon A F G, Leszczynski B. 1998. Phenol oxidising enzymes in the grain aphid’s saliva. Entomologia Experimentalis et Applicata, 86, 197–203.
USDA (United States Department of Agriculture). 2020. World Agricultural Production. [2021-02-10]. https://max.book118.com/html/2020/0814/5113004103002331.shtm
Wang D, Liu D G, Shi X Q, Yang Y J, Zhang N, Shang Z M. 2020. Transcriptome profiling revealed potentially important roles of defensive gene expression in the divergence of insect biotypes: A case study with the cereal aphid Sitobion avenae. BMC Genomics, 21, 546.
Wangai A W, Plumb R T, Emden H E. 2000. The effect of sowing date and insecticides on cereal aphid population and barley yellow dwarf virus on barley in Kenya. Journal of Phytopathology, 148, 33–37.
War A R, Taggar G K, Hussain B, Taggar M S, Nair R M, Sharma H C. 2018. Special issue: Using non-model systems to explore plant-pollinator and plant-herbivore interactions: Plant defence against herbivory and insect adaptations. AOB Plants, 10, 1–19.
Will T, van Bel A J E. 2006. Physical and chemical interactions between aphids and plants. Journal of Experimental Botany, 57, 729–737.
Will T, van Bel A J E. 2008. Induction as well as suppression: How aphid saliva may exert opposite effects on plant defense. Plant Signaling and Behavior, 3, 427–430.
Xiao D, Yang T, Desneux N, Han P, Gao X W. 2015. Assessment of sublethal and transgenerational effects of pirimicarb on the wheat aphids Rhopalosiphum padi and Sitobion avenae. PLoS ONE, 10, e0128936.
Xu Z H, Chen J L, Cheng D F, Sun J R, Liu Y, Francis F. 2011. Discovery of English grain aphid (Hemiptera: Aphididae) biotypes in China. Journal of Economic Entomology, 104, 1080–1086.
Yang Y, Kloos S, Mora-Ramírez I, Romeis J, Brunner S, Li Y H, Meissle M. 2019. Transgenic winter wheat expressing the sucrose transporter HvSUT1 from barley does not affect aphid performance. Insects, 10, 388.
Zadoks J C, Board E. 1974. A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.
Zhang Y, Fan J, Francis F, Chen J L. 2017. Watery saliva secreted by the grain aphid Sitobion avenae stimulates aphid resistance in wheat. Journal of Agricultural and Food Chemistry, 65, 8798–8805.
Zhao R N, He Y Q, Lu Z Y, Chen W L, Zhou C Y, Wang X F, Li T S. 2019. An analysis of the feeding behavior of three stages of Toxoptera citricida by DC electrical penetration graph waveforms. Entomologia Experimentalis et Applicata, 167, 370–376.
Züst T, Agrawal A A. 2016. Mechanisms and evolution of plant resistance to aphids. Nature Plants, 2, 15206.