Soybean resistance to stink bugs (Nezara viridula and Piezodorus guildinii) increases with exposure to solar UV-B radiation and correlates with isoflavonoid content in pods under field conditions

Plant Cell and Environment

Volumn 38, Issue 5, 2015, Pages 920-928

  Zavala, Jorge A ^a,b,d   Mazza, Carlos A ^a,d   Dillon, Francisco M ^a,b,d   Chludil, Hugo D ^a   Ballaré, Carlos L ^a,c,d  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Universidad de Buenos Aires   (Argentina)

^c UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

^d Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Daidzin; Genistin; Isoflavonoids; Plant insect interactions; Pod feeders

Indexed keywords

GLYCINE MAX; HEXAPODA; NEZARA VIRIDULA; PENTATOMIDAE; PIEZODORUS GUILDINII;

DAIDZEIN; GENISTEIN; ISOFLAVONE DERIVATIVE;

ANIMAL; FRUIT; HERBIVORY; HETEROPTERA; METABOLISM; RADIATION RESPONSE; SOYBEAN; ULTRAVIOLET RADIATION;

ANIMALS; FRUIT; GENISTEIN; HERBIVORY; HETEROPTERA; ISOFLAVONES; SOYBEANS; ULTRAVIOLET RAYS;

EID: 84927715962     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12368     Document Type: Article

References (71)

1. Aragon J.R., Molinari A. & Lorenzatti de Diez S. (1997) Manejo integrado de plagas. In El cultivo de soja en la Argentina (eds L.M. Giorda & H.E.J. Baigorri ), pp. 248-288. INTA y SAGPyA, Argentina.
2. Ballaré C.L. (2014) Light and plant defense. Annual Review of Plant Biology 65, 335-363.
3. Ballaré C.L., Caldwell M.M., Flint S.D., Robinson S.A. & Bornman J.F. (2011) Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochemical and Photobiological Sciences 10, 226-241.
4. Ballaré C.L., Mazza C.A., Austin A.T. & Pierik R. (2012) Canopy light and plant health. Plant Physiology 160, 145-165.
5. Beggs C.G. & Wellman E. (1994) Photocontrol of flavonoid biosynthesis. In Photomorphogenesis in Plants (eds A.E. Kendrick & G.H.M. Kronenberg ), pp. 733-751. Kluwer Academic Publishers, Dordrecht, the Netherlands.
6. Bidart-Bouzat M.G. & Imeh-Nathaniel A. (2008) Global change effects on plant chemical defenses against insect herbivores. Journal of Integrative Plant Biology 50, 1339-1354.
7. Bothel D.J., Russin J.S., Wier A.T., Layton M.B., Mink J.S. & Boyd M.L. (2000) Delayed maturity associated with Southern green stink bug (Heteroptera: Pentatomidae) injury at various soybean phenological stages. Journal of Economic Entomology 93, 707-712.
8. Brown B.A., Cloix C., Jiang G.H., Kaiserli E., Herzyk P., Kliebenstein D.J. & Jenkins G.I. (2005) A UV-B-specific signaling component orchestrates plant UV protection. Proceedings of the National Academy of Sciences of the United States of America 102, 18225-18230.
9. Bundy C.S. & McPherson R.M. (2000) Dynamic and seasonal abundance of sink bugs (Heteroptera: Pentatomidae) in cotton-soybean ecosystem. Journal of Economic Entomology 93, 697-706.
10. Caldwell M.M., Ballare C.L., Bornman J.F., Flint S.D., Bjorn L.O., Teramura A.H., ... Tevini M. (2003) Terrestrial ecosystems increased solar ultraviolet radiation and interactions with other climatic change factors. Photochemical and Photobiological Sciences 2, 29-38.
11. Caldwell M.M., Bornman J.F., Ballaré C.L., Flint S.D. & Kulandaivelu G. (2007) Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors. Photochemical and Photobiological Sciences 6, 252-266.
12. Carrao-Panizzi M.C. & Kitamura K. (1995) Isoflavone content in Brazilian soybean cultivars. Breeding Science 45, 295-300.
13. Chimphango S.B.M., Brown C.F., Musil C.F. & Dakora F.D. (2007) Effects of UV-B radiation on seed yield of Glycine max and an assessment of F1 generation progeny for carryover effects. Physiologia Plantarum 131, 378-386.
14. Correa-Ferreira B.S. & de Azevedo J. (2002) Soybean seed damage by different species of stink bugs. Agricultural and Forest Entomology 4, 145-150.
15. Daugherty D.M., Newstandt M.H., Gehrke C.W., Cavanah L.E., Williams L.F. & Green D.E. (1964) An evaluation of damage to soybeans by brown and green stink bugs. Journal of Economic Entomology 57, 719-722.
16. Demkura P.V. & Ballaré C.L. (2012) UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Molecular Plant 5, 642-652.
17. Demkura P.V., Abdala G., Baldwin I.T. & Ballaré C.L. (2010) Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense. Plant Physiology 152, 1084-1095.
18. Dhaubhadel S., Gijzen M., Moy P. & Farhangkhoee M. (2007) Transcriptome analysis reveals a critical role of CHS7 and CHS8 genes for isoflavonoid synthesis in soybean seeds. Plant Physiology 143, 326-338.
19. Dinh T.S., Galis I. & Baldwin I.T. (2013) UVB radiation and HGL-DTGs provide durable resistance against mirid (Tupiocoris notatus) attack in field-grown Nicotiana attenuata plants. Plant, Cell & Environment 36, 590-606.
20. Elliger C.A., Wong Y., Chan B.G. & Waiss A.C. Jr. (1981) Growth inhibitors in tomato (Lycopersicon) to tomato fruitworm (Heliothis zea). Journal of Chemical Ecology 7, 753-758.
21. Fehr W.R., Caviness C.E., Burmood D.T. & Pennington J.S. (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Science 11, 929-931.
22. França Neto J.B., Krzyzanowski F.C. & Costa N.P. (1998) El test de tetrazolio en semillas de soja. EMBRAPA-CNPSo, Londrina. (EMBRAPA-CNPSo. Documentos, 117), Brasil, 72 pp.
23. Heinonen S.M., Wahala K. & Adlercreutz H. (2002) Metabolism of isoflavones in human subjects. Phytochemistry Reviews 1, 175-182.
24. Hoffland E., Dicke M., Van Tintelen W., Dijkman H. & Van Beusichem M.L. (2000) Nitrogen availability and defense of tomato against two-spotted spider mite. Journal of Chemical Ecology 26, 2697-2711.
25. Hoffmann-Campo C.B., Harborne J.B. & McCaffery A.R. (2001) Pre-ingestive and postingestive effects of soya bean extracts and rutin on Trichoplusia ni growth. Entomologia Experimentalis et Applicata 98, 181-194.
26. Hu Z.Q., Zhao H.Y. & Thieme T. (2013) Probing behaviors of Sitobion avenae (Hemiptera: Aphidae) on enhanced UV-B irradiated plants. Archives of Biological Science Belgrade 65, 247-254.
27. Izaguirre M.M., Scopel A.L., Baldwin I.T. & Ballaré C.L. (2003) Convergent responses to stress: solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora. Plant Physiology 132, 1755-1767.
28. Izaguirre M.M., Mazza C.A., Svatos A., Baldwin I.T. & Ballaré C.L. (2007) Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuata and Nicotiana longiflora. Annals of Botany 99, 103-109.
29. Jansen M.A.K., Hectors K., O'Brien N.M., Guisez Y. & Potters G. (2008) Plant stress and human health: do human consumers benefit from UV-B acclimated crops? Plant Science (Shannon, Ireland) 175, 449-458.
30. Koti S., Reddy K.R., Kakani V.G., Zhao D. & Reddy V.R. (2004) Soybean (Glycine max) pollen germination characteristics, flower and pollen morphology in response to enhanced ultraviolet-B radiation. Annals of Botany 94, 855-864.
31. Kotilainen T., Venäläinen T., Tegelberg R., Lindfors A., Julkunen-Tiitto R., Sutinen S., ... Aphalo P.J. (2009) Assessment of UV biological spectral weighting functions for phenolic metabolites and growth responses in silver birch seedlings. Photochemistry and Photobiology 85, 1346-1355.
32. Kuhlmann F. & Müller C. (2009) Development-dependent effects of UV radiation exposure on broccoli plants and interactions with herbivorous insects. Environmental and Experimental Botany 66, 61-68.
33. Kuhlmann F. & Müller C. (2010) UV-B impact on aphid performance mediated by plant quality and plant changes induced by aphids. Plant Biology 12, 676-684.
34. Kuhlmann F. & Müller C. (2011) Impacts of ultraviolet radiation on interactions between plants and herbivorous insects: a chemo-ecological perspective. Progress in Botany 72, 305-347.
35. Lindroth R.L., Hofmann R.W., Campbell B.D., McNabb W.C. & Hunt D.Y. (2000) Population differences in Trifolium repens L. response to ultraviolet-B radiation: foliar chemistry and consequences for two lepidopteran herbivores. Oecologia 122, 20-28.
36. McCloud E.S. & Berenbaum M.R. (1994) Stratospheric ozone depletion and plant-insect interactions: effects of UV-B radiation on foliage quality of Citrus jambhiri for Trichoplusia ni. Journal of Chemical Ecology 20, 525-539.
37. McPherson R.M. (1996) Relationship between soybean maturity group and the phenology and abundance of stink bugs (Heteroptera: Pentatomidae): impact on yield and quality. Journal of Entomological Science 31, 199-208.
38. McPherson R.M., Newsom L.D. & Farthing B.F. (1979) Evaluation of four stink bug species from three genera affecting soybean yield and quality in Louisiana. Journal of Economic Entomology 72, 188-194.
39. McPherson R.M., Todd J.W. & Yeargan K.V. (1994) Stink bugs. In Handbook of Soybean Insect Pests (eds L.G. Higley & D.J. Boethel ), pp. 87-90. Entomol. Soc. Amer., Lanham, MD.
40. Mazza C.A., Zavala J.A., Scopel A.L. & Ballaré C.L. (1999) Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications. Proceedings of the National Academy of Sciences of the United States of America 96, 980-985.
41. Mazza C.A., Boccalandro H.E., Giordano C.V., Battista D., Scopel A.L. & Ballaré C.L. (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiology 122, 117-125.
42. Mazza C.A., Izaguirre M.M., Zavala J.A., Scopel A.L. & Ballaré C.L. (2002) Insect perception of ambient ultraviolet-B radiation. Ecology Letters 5, 722-726.
43. Mazza C.A., Izaguirre M.M., Curiale J. & Ballaré C.L. (2010) A look into the invisible: ultraviolet-B sensitivity in an insect (Caliothrips phaseoli) revealed through a behavioural action spectrum. Proceedings of the Royal Society B 277, 367-373.
44. Mazza C.A., Gimenez P.I., Kantolic A.G. & Ballaré C.L. (2013) Beneficial effects of solar UV-B radiation on soybean yield mediated by reduced insect herbivory under field conditions. Physiologia Plantarum 147, 307-315.
45. Morales L.O., Brosché M., Vainonen J., Jenkins G.I., Wargent J.J., Sipari N., ... Aphalo P.J. (2013) Multiple roles for UV RESISTANCE LOCUS8 in regulating gene expression and metabolite accumulation in Arabidopsis under solar ultraviolet radiation. Plant Physiology 161, 744-759.
46. Musser F.R., Catchot A.L., Gibson B.K. & Knighten K.S. (2011) Economic injury levels for southern green stink bugs (Hemiptera: Pentatomidae) in R7 growth stage soybeans. Crop Protection 30, 63-69.
47. 2 and herbivory on flavonoids of soybean (Glycine max Linnaeus). Journal of Chemical Ecology 36, 35-45.
48. Panizzi A.R. & Slansky F.J. (1985) Rev. of phytophagous pentatomids (Hemiptera: Pentatomidae) associated with soybeans in the Americas. The Florida Entomologist 68, 184-214.
49. Piubelli G.C., Hoffmann-Campo C.B., de Arruda I.C., Franchini J.C. & Lara F.M. (2003a) Flavonoid increase in soybean as a response to Nezara viridula injury and its effect on insect-feeding preference. Journal of Chemical Ecology 29, 1223-1233.
50. Piubelli G.C., Hoffmann-Campo C.B., de Arruda I.C. & Lara F.M. (2003b) Nymphal development, lipid content, growth and weight gain of Nezara viridula (L.) (Heteroptera: Pentatomidae) fed on soybean. Neotropical Entomology 32, 127-132.
51. Piubelli G.C., Hoffmann-Campo C.B., Moscardi F., Miyakubo S.H. & De Oliveira M.C.N. (2005) Are chemical compounds important for soybean resistance to Anticarsia gemmatalis? Journal of Chemical Ecology 31, 1509-1525.
52. Robson T.M., Pancotto V.A., Flint S.D., Ballaré C.L., Sala O.E., Scopel A.L. & Caldwell M.M. (2003) Six years of solar UV-B manipulations affect growth of sphagnum and vascular plants in a Tierra del Fuego peatland. The New Phytologist 160, 379-389.
53. Rousseaux M.C., Ballaré C.L., Scopel A.L., Searles P.S. & Caldwell M.M. (1998) Solar ultraviolet-B radiation affects plant-insect interactions in a natural ecosystem of Tierra del Fuego (southern Argentina). Oecologia 116, 528-535.
54. Rousseaux M.C., Scopel A.L., Searles P.S., Caldwell M.M., Sala O.E. & Ballaré C.L. (2001) Responses to solar ultraviolet-B radiation in a shrub-dominated natural ecosystem of Tierra del Fuego (southern Argentina). Global Change Biology 7, 467-478.
55. Rousseaux M.C., Julkunen-Tiitto R., Searles P.S., Scopel A.L., Aphalo P.J. & Ballaré C.L. (2004) Solar UV-B radiation affects leaf quality and insect herbivory in the southern beech tree Nothofagus antarctica. Oecologia 138, 505-512.
56. Schreiner M., Mewis I., Huyskens-Keil S., Jansen M.A.K., Zrenner R., Winkler J.B., ... Kumbein A. (2012) UV-B-induced secondary plant metabolites: potential benefits for plant and human health. Critical Reviews in Plant Sciences 31, 229-240.
57. Smith J.F., Luttrell R.G. & Greene J.K. (2009) Seasonal abundance, species composition, and population dynamics of stink bugs in production fields of early and late soybean in south Arkansas. Journal of Economic Entomology 102, 229-236.
58. Stamp N.E. & Yang Y.L. (1996) Response of insect herbivores to multiple allelochemicals under different thermal regimes. Ecology 77, 1088-1102.
59. Steele C.L., Gijzen M., Qutob D. & Dixon R.A. (1999) Molecular characterization of the enzyme catalyzing the aryl migration reaction of isoflavonoid biosynthesis in soybean. Archives of Biochemistry and Biophysics 367, 146-150.
60. Stratmann J.W. (2003) Ultraviolet-B radiation co-opts defense signaling pathways. Trends in Plant Science 8, 526-533.
61. Stratmann J.W., Stelmach B.A., Weiler E.W. & Ryan C.A. (2000) UVB/UVA radiation activates a 48kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochemical and Photobiological Sciences 71, 116-123.
62. Temple J.H., Leonard B.R., Davis J. & Fontenot K. (2009) Insecticide efficacy against red banded stink bug, Piezodorus guildinii (Westwood), a new stink bug pest of Louisiana soybean. Midsouth Entomologist 2, 68-69.
63. Teramura A.H., Sullivan J.H. & Lydon J. (1990) Effects of UV-B radiation on soybean yield and seed quality: a 6-year field study. Physiologia Plantarum 80, 5-11.
64. Todd J.W. (1989) Ecology and behaviour of Nezara viridula. Annual Review of Entomology 34, 273-292.
65. Todd J.W. & Turnipseed S.G. (1974) Effects of southern green stink bug damage on yield and quality of soybeans. Journal of Economic Entomology 67, 421-426.
66. Underwood N., Morris W., Gross P. & Lockwood I.I.I.J.R. (2000) Induced resistance to Mexican bean beetles in soybean: variation among genotypes and lack of correlation with constitutive resistance. Oecologia 122, 83-89.
67. Wargent J.J. & Jordan B.R. (2013) From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production. The New Phytologist 197, 1058-1076.
68. Williamson C., Zepp R., Lucas R., Madronich S., Austin A.T., Ballaré C.L., ... Bornman J.F. (2014) Solar ultraviolet radiation in a changing climate. Nature Climate Change 4, June 2014. doi: 10.1038/NCLIMATE2225; in press.
69. Zavala J.A., Scopel A.L. & Ballaré C.L. (2001) Effects of ambient UV-B radiation on soybean crops: impact on leaf herbivory by Anticarsia gemmatalis. Plant Ecology 156, 121-130.
70. Zavala J.A., Casteel C.L., DeLucia E.H. & Berenbaum M.R. (2008) Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects. Proceedings of the National Academy of Sciences of the United States of America 105, 5129-5133.
71. 2. Oecologia 161, 35-41.