Abstract Plant structures and chemicals, which are developed from the shoot apical meristem (SAM), form the main barriers to insect feeding. A plant chimera containing cells of different genetic origins in the SAM will be morphologically and chemically different compared with the parents and thus may result in differential resistance to herbivores. In this study, we explore if particular elements of plant resistance are localized in one of the layers of SAM; the replacement of one cell layer in a chimera may be linked to change of a single resistance trait to herbivores. The morphology and glucosinolate profiles of two periclinal chimeras (labeled as TTC and TCC, respectively) and grafted parents tuber mustard (labeled as TTT) and red cabbage (labeled as CCC) were compared and the performance of whitefly (Bemisia tabaci) in host selection, oviposition preference and development were assessed under controlled conditions. Both chimeras possessed leaf trichomes as parent tuber mustard TTT, however, TTC had significantly more trichomes than TCC and parent TTT. Leaf wax content of both chimeras was intermediate between the two parents. Five aliphatic and two indole glucosinolates were detected in both chimeras, whereas three aliphatic glucosinolates (3-methyl-sulfinylpropyl, 4-methyl-sulfinylbutyl and 2-hydroxy-3-butenyl) were not detected in tuber mustard, and one aliphatic glucosinolate (3-butenyl) was not detected in red cabbage. Unexpectedly for a chimera, the quantities of two aliphatic glucosinolates (3-methyl-sulfinylpropyl and 4-methyl-sulfinylbutyl) in both TTC and TCC were 3- to 5-fold higher than parents. In olfactory preference assays, B. tabaci showed preference to CCC, followed by TCC, TTC and TTT, and number of eggs laid showed the same pattern: CCC>TCC>TTC>TTT. Interestingly, more whiteflies landed on TTT plants than the other three types in a free choice experiment and the developmental duration from egg to adult was the shortest on TTT and increased in the order TTT<TTC<TCC<CCC. Our results indicate plant defenses traits of leaf waxes, trichomes and glucosinolates are not controlled by one cell layer of SAM, but are influenced by interactions amongst cell layers. The overall findings suggest that periclinal chimera systems can be a valuable approach for the study of plant-insect interactions and may also be useful for future resistance breeding.
. Morphology and glucosinolate profiles of chimeric Brassica and the responses of Bemisia tabaci in host selection, oviposition and development[J]. Journal of Integrative Agriculture,
2017, 16(09): 2009-2018.
De Barro P J, Liu S S, Boykin L M, Dinsdale A B. 2011. Bemisia tabaci: A statement of species status. Annual Review of Entomology, 56, 1-19.
Bones A M, Rossiter J T. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry, 67, 1053-1067.
Cao F Q, Liu W X, Wan F H, Cheng L S. 2008. Behavior selection of Bemisia tabaci B-biotype to different host plants and colors. Chinese Bulletin of Entomology, 45, 431-436. (in Chinese)
Chen L P, Ge Y M, Zhu X Y. 2006. Artificial synthesis of interspecific chimeras between tuber mustard (Brassica juncea) and cabbage (Brassica oleracea) and cytological analysis. Plant Cell Reports, 25, 907-913.
Clauss M J, Dietel S, Schubert G, Mitchell-Olds T. 2006. Glucosinolate and trichome defenses in a natural Arabidopsis lyrata population. Journal of Chemical Ecology, 32, 2351-2373.
Clayberg C D. 1975. Insect resistance in a graft-induced periclinal chimera of tomato. HortScience, 10, 13-15.
Cribb B W, Hanan J, Zalucki M P, Perkins L E. 2010. Effects of plant micro-environment on movement of Helicoverpa armigera (Hübner) larvae and the relationship to a hierarchy of stimuli. Arthropod-Plant Interactions, 4, 165-173.
Dicke M, Hilker M. 2003. Induced plant defences: From molecular biology to evolutionary ecology. Basic and Applied Ecology, 4, 3-14.
Du Y J, van Loon J J A, Renwick J A A. 1995. Contact chemoreception of oviposition-stimulating glucosinolates and an oviposition-deterrent cardenolide in two subspecies of Pieris napi. Physiological Entomology, 20, 164-174.
Eigenbrode S D, Stoner K A, Shelton A M, Kain W C. 1991. Characteristics of glossy leaf waxes associated with resistance to diamondback moth (Lepidoptera: Plutellidae) in Brassica oleracea. Journal of Economic Entomology, 84, 1609-1618.
Elbaz M, Halon E, Malka O, Malitsky S, Blum E, Aharoni A, Morin S. 2012. Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Molecular Ecology, 21, 4533-4546.
Elsey K D, Farnham M W. 1994. Response of Brassica oleracea L. to Bemisia tabaci (Gennadius). HortScience, 29, 814-817.
Filippis I, Lopez-Cobollo R, Abbott J, Butcher S, Bishop G J. 2013. Using a periclinal chimera to unravel layer-specific gene expression in plants. The Plant Journal, 75, 1039-1049.
Frank M H, Chitwood D H. 2016. Plant chimeras: The good, the bad, and the ‘Bizzaria’. Development Biology, 419, 41-53.
Goffreda J C, Szymkowiak E J, Sussex I M, Mutschler M A. 1990. Chimeric tomato plants show that aphid resistance and triacylglucose production are epidermal autonomous characters. The Plant Cell, 2, 643-649.
Halkier B A, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology, 57, 303-333.
Hirata Y, Motegi T, Takeda Y, Morikawa K. 2001. Induction of cytoplasmic male sterility in the seed progeny derived from artificially-synthesized interspecific chimera in Brassica. Euphytica, 117, 143-149.
Hopkins R J, van Dam N M, van Loon J J. 2009. Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annual Review of Entomology, 54, 57-83.
Kaddoura R L, Mantell S H. 1991. Synthesis and characterization of Nicotiana solanum graft chimeras. Annals of Botany, 68, 547-556.
Kim G, LeBlanc M L, Wafula E K, dePamphilis C W, Westwood J H. 2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science, 345, 808-811.
Kim J H, Jander G. 2007. Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. The Plant Journal, 49, 1008-1019.
Kim J H, Lee B W, Schroeder F C, Jander G. 2008. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). The Plant Journal, 54, 1015-1026.
Kliebenstein D, Pedersen D, Barker B, Mitchell-Olds T. 2002. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics, 161, 325-332.
Kliebenstein D J. 2004. Secondary metabolites and plant/environment interactions: A view through Arabidopsis thaliana tinged glasses. Plant, Cell & Environment, 27, 675-684.
Krumbein A, Schonhof I, Schreiner M. 2005. Composition and contents of phytochemicals (glucosinolates, carotenoids and chlorophylls) and ascorbic acid in selected Brassica species (B. juncea, B. campestris, B. rapa). Journal of Applied Botany & Food Quality, 79, 168-174.
Li J, Wang Y, Zhang L, Liu B, Cao L, Qi Z, Chen L. 2013. Heritable variation and small RNAs in the progeny of chimeras of Brassica juncea and Brassica oleracea. Journal of Experimental Botany, 64, 4851-4862.
Li L, Li C, Lee G I, Howe G A. 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proceedings of the National Academy of Sciences of the United States of America, 99, 6416-6421.
Liu S S, Colvin J, De Barro P J. 2012. Species concepts as applied to the whitefly Bemisia tabaci systematics: How many species are there? Journal of Integrative Agriculture, 11, 176-186.
Marcotrigiano M. 1986. Experimentally synthesized plant chimeras 3. Qualitative and quantitative characteristics of the flowers of interspecific Nicotiana chimeras. Annals of Botany, 57, 435-442.
Markovich O, Kafle D, Elbaz M, Malitsky S, Aharoni A, Schwarzkopf A, Gershenzon J, Morin S. 2013. Arabidopsis thaliana plants with different levels of aliphatic- and indolyl-glucosinolates affect host selection and performance of Bemisia tabaci. Journal of Chemical Ecology, 39, 1361-1372.
Mewis I, Appel H M, Hom A, Raina R, Schultz J C. 2005. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiology, 138, 1149-1162.
Meyerowitz E M. 1997. Genetic control of cell division patterns in developing plants. Cell, 88, 299-308.
Mithen R. 2001. Glucosinolates - biochemistry, genetics and biological activity. Plant Growth Regulation, 34, 91-103.
Navas-Castillo J, Fiallo-Olive E, Sanchez-Campos S. 2011. Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology, 49, 219-248.
Oliveira M R V, Henneberry T J, Anderson P. 2001. History, current status, and collaborative research projects for Bemisia tabaci. Crop Protection, 20, 709-723.
Pare P W, Tumlinson J H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiology, 121, 325-332.
Pegadaraju V, Louis J, Singh V, Reese J C, Bautor J, Feys B J, Cook G, Parker J E, Shah J. 2007. Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. The Plant Journal, 52, 332-341.
Radcliffe E B, Chapman R K. 1966. Varietal resistance to insect attack in various cruciferous crops. Journal of Economic Entomology, 59, 120-125.
Rasmann S, Agrawal A A. 2009. Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Current Opinion in Plant Biology, 12, 473-478.
Roessingh P, Städler E, Fenwick G R, Lewis J A, Nielsen J K, Hurter J, Ramp T. 1992. Oviposition and tarsal chemoreceptors of the cabbage root fly are stimulated by glucosinolates and host plant extracts. Entomologia Experimentalis et Applicata, 65, 267-282.
Ryan C A, Moura D S. 2002. Systemic wound signaling in plants: A new perception. Proceedings of the National Academy of Sciences of the United States of America, 99, 6519-6520.
Schoonhoven L M, van Loon J J A, Dicke M. 2005. In: Insect-Plant Biology. Oxford, UK. pp. 1-421.
Schuman M C, Baldwin I T. 2016. The layers of plant responses to insect herbivores. Annual Review of Entomology, 61, 373-394.
Schuster D J, Mann R S, Toapanta M, Cordero R, Thompson S, Cyman S, Shurtleff A, Morris II R F. 2010. Monitoring neonicotinoid resistance in biotype B of Bemisia tabaci in Florida. Pest Management Science, 66, 186-195.
Session A, Yanofsky M F, Weigel D. 2000. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science, 289, 779-781.
Simmonds M S J, Blaney W M, Mithen R, Birch A N E, Lewis J. 1994. Behavioural and chemosensory responses of the turnip root fly (Delia floralis) to glucosinolates. Entomologia Experimentalis et Applicata, 71, 41-57.
Städler E, Renwick J A A, Radke C D, Sachdev-Gupta K. 1995. Tarsal contact chemoreceptor response to glucosinolates and cardenolides mediating oviposition in Pieris rape. Physiological Entomology, 20, 175-187.
Sun D B, Liu Y Q, Qin L, Xu J, Li F F, Liu S S. 2013. Competitive displacement between two invasive whiteflies: insecticide application and host plant effects. Bulletin of Entomological Research, 103, 344-353.
Takabayashi J, Dicke M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends in Plant Science, 1, 109-113.
Thieme C J, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W. Yang L, Minambres M, Walther D, Schulze W X, Paz-Ares J, Scheible W R, Kragler F. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants, 1, 15025.
Walling L L. 2008. Avoiding effective defenses: Strategies employed by phloem-feeding insects. Plant Physiology, 146, 859-866.
Wei J N, Yan L H, Ren Q, Li C Y, Ge F, Kang L. 2013. Antagonism between herbivore-induced plant volatiles and trichomes affects tritrophic interactions. Plant, Cell & Environment, 36, 315-327.
Yan J F, Tan M M, Chen C, Wang L, Tan J Z. 2014. Flower color chimera and its application in breeding of ornamental plant. Journal of Anhui Agricultral Sciences, 42, 1600-1602. (in Chinese)
Zang L S, Liu Y Q, Liu S S. 2005. A new clip-cage for whitefly experimental studies. Entomological Knowledge, 42, 329-331. (in Chinese)
Zhou J, Hirata Y, Nou I S, Shiotani H, Ito T. 2002. Interactions between different genotypic tissues in citrus graft chimeras. Euphytica, 126, 355-364.
Zukalova H, Vasak J. 2002. The role and effects of glucosinolates of Brassica species - A review. Rostlinna Vyroba, 48, 175-180.