全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Insect Attraction versus Plant Defense: Young Leaves High in Glucosinolates Stimulate Oviposition by a Specialist Herbivore despite Poor Larval Survival due to High Saponin Content

DOI: 10.1371/journal.pone.0095766

Full-Text   Cite this paper   Add to My Lib

Abstract:

Glucosinolates are plant secondary metabolites used in plant defense. For insects specialized on Brassicaceae, such as the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), glucosinolates act as “fingerprints” that are essential in host plant recognition. Some plants in the genus Barbarea (Brassicaceae) contain, besides glucosinolates, saponins that act as feeding deterrents for P. xylostella larvae, preventing their survival on the plant. Two-choice oviposition tests were conducted to study the preference of P. xylostella among Barbarea leaves of different size within the same plant. P. xylostella laid more eggs per leaf area on younger leaves compared to older ones. Higher concentrations of glucosinolates and saponins were found in younger leaves than in older ones. In 4-week-old plants, saponins were present in true leaves, while cotyledons contained little or no saponins. When analyzing the whole foliage of the plant, the content of glucosinolates and saponins also varied significantly in comparisons among plants that were 4, 8, and 12 weeks old. In Barbarea plants and leaves of different ages, there was a positive correlation between glucosinolate and saponin levels. This research shows that, in Barbarea plants, ontogenetical changes in glucosinolate and saponin content affect both attraction and resistance to P. xylostella. Co-occurrence of a high content of glucosinolates and saponins in the Barbarea leaves that are most valuable for the plant, but are also the most attractive to P. xylostella, provides protection against this specialist herbivore, which oviposition behavior on Barbarea seems to be an evolutionary mistake.

References

[1]  Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH, editors. Herbivores: Their Interactions with Secondary Plant Metabolites. New York, USA: Academic Press. 3–54.
[2]  McKey D (1974) Adaptive patterns in alkaloid physiology. American Naturalist 108: 305–320. doi: 10.1086/282909
[3]  Harper JL (1989) The value of a leaf. Oecologia 80: 53–58. doi: 10.1007/bf00789931
[4]  Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62: 471–481. doi: 10.1016/s0031-9422(02)00549-6
[5]  van Dam NM, de Jong TJ, Iwasa Y, Kubo T (1996) Optimal distribution of defences: are plants smart investors? Functional Ecology 10: 128–136. doi: 10.2307/2390271
[6]  Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57: 303–333. doi: 10.1146/annurev.arplant.57.032905.105228
[7]  Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annual Review of Entomology 54: 57–83. doi: 10.1146/annurev.ento.54.110807.090623
[8]  Petersen B, Chen S, Hansen C, Olsen C, Halkier B (2002) Composition and content of glucosinolates in developing Arabidopsis thaliana. Planta 214: 562–571. doi: 10.1007/s004250100659
[9]  Gutbrodt B, Dorn S, Unsicker S, Mody K (2012) Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry. Chemoecology 22: 101–111. doi: 10.1007/s00049-012-0102-1
[10]  Lambdon PW, Hassall M, Boar RR, Mithen R (2003) Asynchrony in the nitrogen and glucosinolate leaf-age profiles of Brassica: is this a defensive strategy against generalist herbivores? Agriculture, Ecosystems & Environment 97: 205–214. doi: 10.1016/s0167-8809(03)00036-7
[11]  Shelton AL (2005) Within-plant variation in glucosinolate concentrations of Raphanus sativus across multiple scales. Journal of Chemical Ecology 31: 1711–1732. doi: 10.1007/s10886-005-5922-9
[12]  Wentzell AM, Kliebenstein DJ (2008) Genotype, age, tissue, and environment regulate the structural outcome of glucosinolate activation. Plant Physiology 147: 415–428. doi: 10.1104/pp.107.115279
[13]  Osbourn A (1996) Saponins and plant defence – a soap story. Trends in Plant Science 1: 4–9. doi: 10.1016/s1360-1385(96)80016-1
[14]  Francis G, Kerem Z, Makkar HPS, Becker K (2002) The biological action of saponins in animal systems: a review. British Journal of Nutrition 88: 587–605. doi: 10.1079/bjn2002725
[15]  Sparg SG, Light ME, van Staden J (2004) Biological activities and distribution of plant saponins. Journal of Ethnopharmacology 94: 219–243. doi: 10.1016/j.jep.2004.05.016
[16]  Matsuda K, Kaneko M, Kusaka K, Shishido T, Tamaki Y (1999) Soyasaponins as feeding stimulants to the oriental clouded yellow larva, Colias erate poliographus (Lepidoptera: Pieridae). Applied Entomology and Zoology 33: 255–258.
[17]  Adel M, Sehnal F, Jurzysta M (2000) Effects of alfalfa saponins on the moth Spodoptera littoralis. Journal of Chemical Ecology 26: 1065–1078. doi: 10.1023/a:1005445217004
[18]  Jain DC, Tripathi AK (1991) Insect feeding-deterrent activity of some saponin glycosides. Phytotherapy Research 5: 139–141. doi: 10.1002/ptr.2650050311
[19]  De Geyter E, Swevers L, Caccia S, Geelen D, Smagghe G (2012) Saponins show high entomotoxicity by cell membrane permeation in Lepidoptera. Pest Management Science 68: 1199–1205. doi: 10.1002/ps.3284
[20]  Potter D, Kimmerer T (1989) Inhibition of herbivory on young holly leaves: evidence for the defensive role of saponins. Oecologia 78: 322–329. doi: 10.1007/bf00379105
[21]  Pecetti L, Biazzi E, Tava A (2010) Variation in saponin content during the growing season of spotted medic Medicago arabica (L.) Huds. Journal of the Science of Food and Agriculture 90: 2405–2410. doi: 10.1002/jsfa.4099
[22]  Szakiel A, P?czkowski C, Henry M (2011) Influence of environmental abiotic factors on the content of saponins in plants. Phytochemistry Reviews 10: 471–491. doi: 10.1007/s11101-010-9177-x
[23]  Teng H-M, Fang M-F, Cai X, Hu Z-H (2009) Localization and dynamic change of saponin in vegetative organs of Polygala tenuifolia. Journal of Integrative Plant Biology 51: 529–536. doi: 10.1111/j.1744-7909.2009.00830.x
[24]  Agerbirk N, Olsen CE, Bibby BM, Frandsen HO, Brown LD, et al. (2003) A saponin correlated with variable resistance of Barbarea vulgaris to the diamondback moth Plutella xylostella. Journal of Chemical Ecology 29: 1417–1433.
[25]  Shinoda T, Nagao T, Nakayama M, Serizawa H, Koshioka M, et al. (2002) Identification of a triterpenoid saponin from a crucifer, Barbarea vulgaris, as a feeding deterrent to the diamondback moth, Plutella xylostella. Journal of Chemical Ecology 28: 587–599.
[26]  Nielsen JK, Nagao T, Okabe H, Shinoda T (2010) Resistance in the plant, Barbarea vulgaris, and counter-adaptations in flea beetles mediated by saponins. Journal of Chemical Ecology 36: 277–285. doi: 10.1007/s10886-010-9758-6
[27]  Nielsen NJ, Nielsen J, Staerk D (2010) New resistance-correlated saponins from the insect-resistant crucifer Barbarea vulgaris. Journal of Agricultural and Food Chemistry 58: 5509–5514. doi: 10.1021/jf903988f
[28]  Badenes-Perez FR, Reichelt M, Gershenzon J, Heckel DG (2014) Using plant chemistry and insect preference to study the potential of Barbarea (Brassicaceae) as a dead-end trap crop for diamondback moth (Lepidoptera: Plutellidae). Phytochemistry: 137–144.
[29]  Nielsen JK, de Jong PW (2005) Temporal and host-related variation in frequencies of genes that enable Phyllotreta nemorum to utilize a novel host plant, Barbarea vulgaris. Entomologia Experimentalis Et Applicata 115: 265–270. doi: 10.1111/j.1570-7458.2005.00293.x
[30]  Agerbirk N, Olsen CE, Nielsen JK (2001) Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58: 91–100. doi: 10.1016/s0031-9422(01)00151-0
[31]  Talekar NS, Shelton AM (1993) Biology, ecology, and management of the diamondback moth. Annual Review of Entomology 38: 275–301. doi: 10.1146/annurev.en.38.010193.001423
[32]  Furlong MJ, Wright DJ, Dosdall LM (2013) Diamondback moth ecology and management: problems, progress, and prospects. Annual Review of Entomology 58: 517–541. doi: 10.1146/annurev-ento-120811-153605
[33]  Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J (2002) Disarming the mustard oil bomb. Proceedings of the National Academy of Sciences of the United States of America 99: 11223–11228. doi: 10.1073/pnas.172112899
[34]  Badenes-Perez FR, Reichelt M, Gershenzon J, Heckel DG (2011) Phylloplane location of glucosinolates in Barbarea spp. (Brassicaceae) and misleading assessment of host suitability by a specialist herbivore. New Phytologist 189: 549–556. doi: 10.1111/j.1469-8137.2010.03486.x
[35]  van Loon JJA, Wang CZ, Nielsen JK, Gols R, Qiu YT (2002) Flavonoids from cabbage are feeding stimulants for diamondback moth larvae additional to glucosinolates: chemoreception and behaviour. Entomologia Experimentalis et Applicata 104: 27–34. doi: 10.1046/j.1570-7458.2002.00987.x
[36]  Spencer JL, Pillai S, Bernays EA (1999) Synergism in the oviposition behavior of Plutella xylostella: sinigrin and wax compounds. Journal of Insect Behavior 12: 483–500.
[37]  Renwick JAA, Haribal M, Gouinguené S, Stadler E (2006) Isothiocyanates stimulating oviposition by the diamondback moth, Plutella xylostella. Journal of Chemical Ecology 32: 755–766. doi: 10.1007/s10886-006-9036-9
[38]  Badenes-Perez FR, Reichelt M, Heckel DG (2010) Can sulfur fertilisation increase the effectiveness of trap crops for diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae)? Pest Management Science 66: 832–838. doi: 10.1002/ps.1949
[39]  Idris AB, Grafius E (1996) Effects of wild and cultivated host plants on oviposition, survival, and development of diamondback moth (Lepidoptera: Plutellidae) and its parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae). Environmental Entomology 25: 825–833.
[40]  Shelton AM, Nault BA (2004) Dead-end trap cropping: a technique to improve management of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Crop Protection 23: 497–503. doi: 10.1016/j.cropro.2003.10.005
[41]  Lu JH, Liu SS, Shelton AM (2004) Laboratory evaluations of a wild crucifer Barbarea vulgaris as a management tool for the diamondback moth Plutella xylostella (Lepidoptera : Plutellidae). Bulletin of Entomological Research 94: 509–516. doi: 10.1079/ber2004328
[42]  Badenes-Perez FR, Shelton AM, Nault BA (2004) Evaluating trap crops for diamondback moth, Plutella xylostella (Lepidoptera : Plutellidae). Journal of Economic Entomology 97: 1365–1372. doi: 10.1603/0022-0493-97.4.1365
[43]  Shelton AM, Badenes-Perez FR (2006) Concepts and applications of trap cropping in pest management. Annual Review of Entomology 51: 285–308. doi: 10.1146/annurev.ento.51.110104.150959
[44]  Badenes-Perez FR, Nault BA, Shelton AM (2006) Dynamics of diamondback moth oviposition in the presence of a highly preferred non-suitable host. Entomologia Experimentalis et Applicata 120: 23–31. doi: 10.1111/j.1570-7458.2006.00416.x
[45]  Raupp MJ, Denno RF (1983) Leaf age as a predictor of herbivore distribution and abudance. In: Denno RF, McClure MS, editors. Variable plants and herbivores in natural and managed systems. New York, NY: Academic Press. 91–124.
[46]  Raupp MJ, Werren JH, Sadof CS (1988) Effects of short-term phenological changes in leaf suitability on the survivorship, growth, and development of gypsy moth (Lepidoptera: Lymantriidae) larvae. Environmental Entomology 17: 316–319.
[47]  Kause A, Ossipov V, Haukioja E, Lempa K, Hanhim?ki S, et al. (1999) Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120: 102–112. doi: 10.1007/s004420050838
[48]  King BH, Crowe ML, Blackmore MD (1998) Effects of leaf age on oviposition and on offspring fitness in the imported willow leaf beetle Plagiodera versicolora (Coleoptera: Chrysomelidae). Journal of Insect Behavior 11: 23–36.
[49]  Karban R (1990) Herbivore outbreaks on only young trees: testing hypotheses about aging and induced resistance. Oikos 59: 27–32. doi: 10.2307/3545118
[50]  Heisswolf A, Obermaier E, Poethke HJ (2005) Selection of large host plants for oviposition by a monophagous leaf beetle: nutritional quality or enemy-free space? Ecological Entomology 30: 299–306. doi: 10.1111/j.0307-6946.2005.00706.x
[51]  Spangler SM, Calvin DD (2000) Influence of sweet corn growth stages on European corn borer (Lepidoptera: Crambidae) oviposition. Environmental Entomology 29: 1226–1235. doi: 10.1603/0046-225x-29.6.1226
[52]  Badenes-Perez FR, Nault BA, Shelton AM (2005) Manipulating the attractiveness and suitability of hosts for diamondback moth (Lepidoptera : Plutellidae). Journal of Economic Entomology 98: 836–844. doi: 10.1603/0022-0493-98.3.836
[53]  St?dler E, Baur R, De Jong R (2002) Sensory basis of host-plant selection: in earch of the “fingerprints” related to oviposition of the cabbage root fly. Acta Zoologica Academiae Scientiarum Hungaricae 48 (Suppl. 1)265–280.
[54]  Renwick JAA (1989) Chemical ecology of oviposition in phytophagous insects. Experientia 45: 223–228. doi: 10.1007/bf01951807
[55]  Janz N (2002) Evolutionary ecology and oviposition strategies. In: Hilker M, Meiners T, editors. Chemoecology of Insect Eggs and Egg Deposition. Oxford, UK: Blackwell Publishing Ltd. 349–376.
[56]  Larsson S, Ekbom B (1995) Oviposition mistakes in herbivorous insects: confusion or a step towards a new host plant? Oikos 72: 155–160. doi: 10.2307/3546051
[57]  Thompson JN (1999) What we know and do not know about coevolution: insect herbivores and plants as a test case. In: Olff H, Brown VK, Drent RH, editors. Herbivores: Between Plants and Predators. Oxford, UK: Blackwell Science Ltd. 7–30.
[58]  Zhang P-J, Lu Y-b, Zalucki M, Liu S-S (2012) Relationship between adult oviposition preference and larval performance of the diamondback moth, Plutella xylostella. Journal of Pest Science 85: 247–252. doi: 10.1007/s10340-012-0425-2
[59]  Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution 20: 441–448. doi: 10.1016/j.tree.2005.05.001
[60]  Wallace SK, Eigenbrode SD (2002) Changes in the glucosinolate–myrosinase defense system in Brassica juncea cotyledons during seedling development. Journal of Chemical Ecology 28: 243–256.
[61]  Uematsu H (1996) Inter-leaf movement of larvae of diamondback moth, Plutella xylostella L. (Lepidoptera: Yponomeutidae) on rape (Brassica napus) seedlings. Japanese Journal of Applied Entomology and Zoology 40: 35–38. doi: 10.1303/jjaez.40.35
[62]  Root RB, Tahvanainen J (1969) Role of winter cress, Barbarea vulgaris, as a temporary host in seasonal development of crucifer fauna. Annals of the Entomological Society of America 62: 852–855.
[63]  Feeny P (1976) Plant apparency and chemical defense. In: Wallace J, Mansell R, editors. Biochemical Interaction Between Plants and Insects: Springer US. 1–40.
[64]  Feeny P (1977) Defensive Ecology of the Cruciferae. Annals of the Missouri Botanical Garden 64: 221–234. doi: 10.2307/2395334
[65]  van Leur H, Raaijmakers CE, van Dam NM (2006) A heritable glucosinolate polymorphism within natural populations of Barbarea vulgaris. Phytochemistry 67: 1214–1223. doi: 10.1016/j.phytochem.2006.04.021
[66]  Pivnick KA, Jarvis BJ, Gillott C, Slater GP, Underhill EW (1990) Daily patterns of reproductive activity and the influence of adult density and exposure to host plants on reproduction in the diamondback moth (Lepidoptera: Plutellidae). Environmental Entomology 19: 587–593.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133