High-throughput phenotyping of plant resistance to aphids by automated video tracking

Plant Methods

Maarten A Jongsma¹  Marcel Dicke²  Lucas PJJ Noldus³  Olga E Krips³  Gerrie L Wiegers¹  Marianne Hanhart-van den Brink²  Manus PM Thoen¹  Cindy JM ten Broeke²  Karen J Kloth¹ 

[1] Plant Research International, Wageningen University and Research Center, Wageningen, 6700, AA, The Netherlands;Laboratory of Entomology, Wageningen University, Wageningen, 6700, AA, The Netherlands;Noldus Information Technology bv, Wageningen, 6700, AG, The Netherlands

关键词: Arabidopsis thaliana;    Piercing-sucking insects;    Phenotyping;    Lactuca sativa;    Host plant resistance;    Automated video tracking;    Arabidopsis;    Aphids;   

Others  :  1225052
DOI  :  10.1186/s13007-015-0044-z

 received in 2014-10-16, accepted in 2015-01-05,  发布年份 2015

【 摘 要 】

Background

Piercing-sucking insects are major vectors of plant viruses causing significant yield losses in crops. Functional genomics of plant resistance to these insects would greatly benefit from the availability of high-throughput, quantitative phenotyping methods.

Results

We have developed an automated video tracking platform that quantifies aphid feeding behaviour on leaf discs to assess the level of plant resistance. Through the analysis of aphid movement, the start and duration of plant penetrations by aphids were estimated. As a case study, video tracking confirmed the near-complete resistance of lettuce cultivar ‘Corbana’ against Nasonovia ribisnigri (Mosely), biotype Nr:0, and revealed quantitative resistance in Arabidopsis accession Co-2 against Myzus persicae (Sulzer). The video tracking platform was benchmarked against Electrical Penetration Graph (EPG) recordings and aphid population development assays. The use of leaf discs instead of intact plants reduced the intensity of the resistance effect in video tracking, but sufficiently replicated experiments resulted in similar conclusions as EPG recordings and aphid population assays. One video tracking platform could screen 100 samples in parallel.

Conclusions

Automated video tracking can be used to screen large plant populations for resistance to aphids and other piercing-sucking insects.

【 授权许可】

   
2015 Kloth et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Blackman RL, Eastop VF. Aphids on the world’s herbaceous plants and schrubs. John Wiley & Sons, Ltd. & Natural History Museum, London; 2006.
• [2]Tjallingii WF. Regulation of phloem sap feeding by aphids. In: Regulatory mechanisms in insect feeding. Chapman RF, De Boer G, editors. Springer, US; 1995: p.190-209.
• [3]Minks AK, Harrewijn P. World crop pests. Aphids. Their biology, Natural enemies and control. Elsevier Science Publishers, Amsterdam, the Netherlands; 1989.
• [4]De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CMJ. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. MPMI. 2005; 18:923-37.
• [5]Eigenbrode SD, Espelie KE. Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol. 1995; 40:171-94.
• [6]Wang E, Wang R, DeParasis J, Loughrin JH, Gan S, Wagner GJ. Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat Biotechnol. 2001; 19:371-4.
• [7]Ceci LR, Volpicella M, Rahbé Y, Gallerani R, Beekwilder J, Jongsma MA. Selection by phage display of a variant mustard trypsin inhibitor toxic against aphids. Plant J. 2003; 33:557-66.
• [8]Mewis I, Appel HM, Hom A, Raina R, Schultz JC. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol. 2005; 138:1149-62.
• [9]Smith CM, Boyko EV. The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl. 2007; 122:1-16.
• [10]Pegadaraju V, Louis J, Singh V, Reese JC, Bautor J, Feys BJ, Cook G, Parker JE, Shah J. Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. Plant J. 2007; 52:332-41.
• [11]Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol. 1998; 24:1355-68.
• [12]Will T, van Bel AJE. Physical and chemical interactions between aphids and plants. J Exp Bot. 2006; 57:729-37.
• [13]Kollner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J. A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell. 2008; 20:482-94.
• [14]Wink M. Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet. 1988; 75:225-33.
• [15]Eenink AH, Dieleman FL. Screening Lactuca for resistance to Myzus persicae. Neth J Plant Pathol. 1977; 83:139-51.
• [16]Smyrnioudis IN, Harrington R, Katis NI. A simple test for evaluation of transmission efficiency of barley yellow dwarf virus by aphids. Phytoparasitica. 2002; 30:535-8.
• [17]Chen X, Vosman B, Visser RGF, van der Vlugt RAA, Broekgaarden C. High throughput phenotyping for aphid resistance in large plant collections. Plant Methods. 2012; 8:33. BioMed Central Full Text
• [18]Stelinski L, Tiwari S. Vertical T-maze choice assay for arthropod response to odorants. J Vis Exp. 2013; 72:e50229.
• [19]Kloth KJ, Thoen MPM, Bouwmeester HJ, Jongsma MA, Dicke M. Association mapping of plant resistance to insects. Trends Plant Sci. 2012; 17:311-9.
• [20]Smith CM, Khan ZR, Pathak MD. Techniques for evaluating insect resistance in crop plants. CRC Press LLC, Florida; 1994.
• [21]Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, Vosman B. Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ. 2008; 31:1592-605.
• [22]Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J. Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry. 2006; 67:2450-62.
• [23]Moran PJ, Thompson GA. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 2001; 125:1074-85.
• [24]McLean DL, Kinsey MG. A technique for electronically recording aphid feeding and salivation. Nature. 1964; 202:1358-9.
• [25]Tjallingii WF. Electrical recording of stylet penetration activities. In: Aphids, their biology, natural enemies and control. Minks AK, Harrewijn P, editors. Elsevier, Amsterdam; 1988: p.95-108.
• [26]van Emden HF, Harrington R. Aphids as crop pests. CABI, Oxfordshire, UK; 2007.
• [27]van Helden M, Tjallingii WF. Tissue localisation of lettuce resistance to the aphid N. ribisnigri using electrical penetration graphs. Entomol Exp Appl. 1993; 68:269-78.
• [28]Tjallingii WF. Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot. 2006; 57:739-45.
• [29]Will T, Tjallingii WF, Thönnessen A, Van Bel AJE. Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci U S A. 2007; 104:10536-41.
• [30]Boquel S, Giordanengo P, Ameline A. Divergent effects of PVY-infected potato plant on aphids. Eur J Plant Pathol. 2011; 129:507-10.
• [31]Nalam VJ, Keeretaweep J, Sarowar S, Shah J. Root-derived oxylipins promote green peach aphid performance on arabidopsis foliage. Plant Cell. 2012; 24:1643-53.
• [32]ten Broeke CJM, Dicke M, van Loon JJA. Resistance in a Lactuca virosa accession to a new biotype of Nasonovia ribisnigri. Euphytica. 2013; 193:265-75.
• [33]Alvarez AE, Tjallingii WF, Garzo E, Vleeshouwers V, Dicke M, Vosman B. Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomol Exp Appl. 2006; 121:145-57.
• [34]ten Broeke CJM, Dicke M, van Loon JJA. Performance and feeding behaviour of two biotypes of the black currant-lettuce aphid, Nasonovia ribisnigri, on resistant and susceptible Lactuca sativa near-isogenic lines. Bull Entomol Res. 2013; 103:511-21.
• [35]Bakchine E, Pham-Delegue MH, Kaiser L, Masson C. Brief communication: computer analysis of the exploratory behavior of insects and mites in an olfactometer. Physiol Behav. 1990; 48:183-7.
• [36]Shcherbakov D, Schill RO, Brümmer F, Blum M. Movement behaviour and video tracking of Milnesium tardigradum Doyère, 1840 (Eutardigrada, Apochela). Contrib Zool. 2010; 79:33-8.
• [37]Pinkiewicz TH, Purser GJ, Williams RN. A computer vision system to analyse the swimming behaviour of farmed fish in commercial aquaculture facilities: a case study using cage-held atlantic salmon. Aquac Eng. 2011; 45:20-7.
• [38]Moreno-Delafuente A, Garzo E, Moreno A, Fereres A. A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLoS ONE. 2013; 8:e61543.
• [39]Spitzen J, Spoor CW, Grieco F, ter Braak C, Beeuwkes J, van Brugge SP, Kranenbarg S, Noldus LPJJ, van Leeuwen JL, Takken W. A 3D analysis of flight behavior of Anopheles gambiae sensu stricto malaria mosquitoes in response to human odor and heat. PLoS ONE. 2013; 8:e62995.
• [40]Dell AI, Bender JA, Branson K, Couzin ID, de Polavieja GG, Noldus LPJJ, Pérez-Escudero A, Perona P, Straw AD, Wikelski M, Brose U. Automated image-based tracking and its application in ecology. Trends Ecol Evol. 2014; 29:417-28.
• [41]Noldus LPJJ, Spink AJ, Tegelenbosch RAJ. Computerised video tracking, movement analysis and behaviour recognition in insects. Comput Electron Agric. 2002; 35:201-27.
• [42]Tjallingii WF. Sieve element acceptance by aphids. Eur J Entomol. 1994; 91:47-52.
• [43]Prado E, Tjallingii WF. Behavioral evidence for local reduction of aphid-induced resistance. J Insect Sci. 2007; 7:1-8.
• [44]Grieco F, Loijens L, Krips OE, Smit G, Spink AJ, Zimmerman P. EthoVision XT reference manual. Noldus Information Technology, Wageningen; 2010.
• [45]Will T, Kornemann SR, Furch ACU, Tjallingii WF, van Bel AJE. Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? J Exp Biol. 2009; 212:3305-12.
• [46]Reinink K, Dieleman FL. Comparison of sources of resistance to leaf aphids in lettuce (lactuca sativa L.). Euphytica. 1989; 40:21-9.
• [47]Ten Broeke CJM. Unravelling the resistance mechanism of lettuce against Nasonovia ribisnigri . Wageningen University, Wageningen; 2013.
• [48]Liu Y, McCreight JD. Responses of Nasonovia ribisnigri (Homoptera: Aphididae) to susceptible and resistant lettuce. J Econ Entomol. 2006; 99:972-8.
• [49]Leon J, Rojo E, Sanchez-Serrano JJ. Wound signalling in plants. J Exp Bot. 2001; 52:1-9.
• [50]Will T, Hewer A, Van Bel AJE. A novel perfusion system shows that aphid feeding behaviour is altered by decrease of sieve-tube pressure. Entomol Exp Appl. 2008; 127:237-45.
• [51]Mittler TE. Applications of artificial feeding techniques for aphids. In: Aphids, their biology, natural enemies ano control. Minks AK, Harrewijn P, editors. Elsevier, Amsterdam; 1988: p.145-70.
• [52]Turgeon R. The puzzle of phloem pressure. Plant Physiol. 2010; 154:578-81.
• [53]Martin B, Rahbé Y, Fereres A. Blockage of stylet tips as the mechanism of resistance to virus transmission by Aphis gossypii in melon lines bearing the Vat gene. Ann Appl Biol. 2003; 142:245-50.
• [54]Husson SJ, Steuer Costa W, Schmitt C, Gottschalk A.Keeping track of worm trackers [INTERNET]. http://www.wormbook.org . Available from: [http://www.wormbook.org] webcite Wormbook.1-17.
• [55]Noldus LPJJ, Spink AJ, Tegelenbosch RAJ. EthoVision: a versatile video tracking system for automation of behavioral experiments. Behav Res Methods Instrum Comput. 2001; 33:398-414.
• [56]Hardie J, Holyoak M, Taylor NJ, Griffiths DC. The combination of electronic monitoring and video-assisted observations of plant penetration by aphids and behavioural effects of polygodial. Entomol Exp Appl. 1992; 62:233-9.
• [57]Hardie J, Powell G. Close-up video combined with electronic monitoring of plant penetration and behavioral effects of an aphid (Homoptera: Aphididae) antifeedant. In: Principles and applications of electronic monitoring and other techniques in the study of Homopteran feeding behavior. Walker PG, Backus EA, editors. Entomological Society of America, US; 2000: p.201-11.
• [58]R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013.