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Plant Molecular Biology Reporter

, Volume 33, Issue 3, pp 377–387 | Cite as

(Z)-3-Hexenal, One of the Green Leaf Volatiles, Increases Susceptibility of Rice to the White-Backed Planthopper Sogatella furcifera

  • Baohui Wang
  • Guoxin Zhou
  • Zhaojun Xin
  • Rui Ji
  • Yonggen Lou
Original Paper

Abstract

Green leaf volatiles (GLVs), the products of the hydroperoxide lyase (HPL) branch of the oxylipin pathway, play important roles in plant defense responses to both insect pests and pathogens. However, little is known about the role of GLVs in the defense responses of rice to the white-backed planthopper (WBPH, Sogatella furcifera (Horváth)). Here, we found that the rice HPL gene OsHPL3 was upregulated in response to infestation by WBPH adults and nymphs. Using an Agrobacterium-mediated transformation system, we obtained two homozygous lines with an antisense expression vector of OsHPL3 (as-hpl) and a single insertion that reduced the gene’s expression by 48.31–52.56 %. Biochemical assays revealed that as-hpl lines had lower wound-induced GLV levels, mainly (Z)-3-hexenal, (Z)-3-hexen-1-ol, and (E)-2-hexenal, but higher JA levels, compared to wild-type (WT) plants. Biological assays showed that WBPH adult females and nymphs preferred to settle and/or oviposit on WT plants, where they survived better than on as-hpl plants. In addition, both male and female WBPH nymphs fed on as-hpl plants performed less well: they developed more slowly, and pairs subsequently laid fewer eggs compared to pairs fed on WT plants. The enhanced resistance of as-hpl plants to WBPH infestation mainly correlated with lower levels of GLVs, especially (Z)-3-hexenal. Collectively, these results indicated that WBPH infestation may enhance the susceptibility of rice by inducing the release of (Z)-3-hexenal.

Keywords

Rice Sogatella furcifera Green leaf volatile (Z)-3-hexenal Hydroperoxide lyase Defense response 

Abbreviations

as-hpl line

A line with antisense expression of OsHPL3

BPH

Brown planthopper Nilaparvata lugens (Stål)

GLVs

Green leaf volatiles

HPL

Hydroperoxide lyase

JA

Jasmonic acid

qRT-PCR

Quantitative real-time polymerase chain reaction

SA

Salicylic acid

SSB

Striped stem borer Chilo suppressalis

WBPH

White-backed planthopper Sogatella furcifera (Horváth)

WT

Wild-type

Xoo

The bacterial blight Xanthomonas oryzae pv. oryzae

Notes

Acknowledgments

We thank Emily Wheeler for editorial assistance. The study was jointly sponsored by the National Basic Research Program of China (2010CB126200), the National Program of Transgenic Variety Development of China (2011ZX08001-001), the National Natural Science Foundation of China (31101451), and the China Agriculture Research System (CARS-01-21).

Supplementary material

11105_2014_756_MOESM1_ESM.doc (38 kb)
Appendix S1 Primers and probes used for qRT-PCR of target genes. (DOC 38 kb)
11105_2014_756_MOESM2_ESM.doc (208 kb)
Appendix S2 cDNA and deduced amino acid sequence of rice OsHPL3 gene (AY340220). Start and stop codes (in red boxes) and region used for antisense transformation (red letters) are shown. (DOC 207 kb)
11105_2014_756_MOESM3_ESM.doc (75 kb)
Appendix S3 Rice transformation vector pCAMBIA-HPL (13.7 kb) with hyg and gus as plant selectable marker genes. (DOC 75 kb)
11105_2014_756_MOESM4_ESM.doc (37 kb)
Appendix S4 DNA gel-blot analysis of one WT line and two as-hpl T2 lines (L7-5 and L11-4). Genomic DNA was digested with EcoR I (E) or Xba I (X). The blot was hybridized with a probe (about 0.7 kb) specific for reporter gene gus. Hybridization was created using the DIG High Prime DNA Labeling and Detection Starter Kit II. All the as-hpl lines had a single insertion of the transgene. (DOC 37 kb)
11105_2014_756_MOESM5_ESM.doc (14.6 mb)
Appendix S5 Growth phenotypes of as-hpl lines and WT plants. There were no significant differences in two-week-old seedlings and plants at the tillering and heading stages between the as-hpl lines and WT plants. (DOC 14923 kb)
11105_2014_756_MOESM6_ESM.doc (100 kb)
Appendix S6 Expression levels (+SE) of OsHPL3 in stems of WT plants and two as-hpl lines without treatment and 12 h after mechanical wounding. There were significant differences between as-hpl lines and WT plants at 12 h (n = 5, Student’s t-test). Wound-induced transcript levels of OsHPL3 in L7-5 and L11-4 were about 47.44 and 51.69 % of those in WT plants 12 h after mechanical wounding. (DOC 99.5 kb)
11105_2014_756_MOESM7_ESM.doc (66 kb)
Appendix S7 Mean transcript levels (+SE) of OsHI-LOX (A), OsAOS1 (B), OsAOS2 (C) in as-hpl lines and WT plants after infestation by WBPH (n = 3-5). Letters indicate significant differences among treatments (P ≤ 0.05, Duncan’s multiple-range test). (DOC 66 kb)

References

  1. Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075–1078CrossRefPubMedGoogle Scholar
  2. Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J (2000) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277(2):305–310CrossRefPubMedGoogle Scholar
  3. Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. BBA-Mol Cell Biol L 1734:91–111Google Scholar
  4. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant–plant interactions: ‘talking trees’ in the genomics era. Science 331:812–815CrossRefGoogle Scholar
  5. Bate NJ, Rothstein SJ (1998) C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16:561–569CrossRefPubMedGoogle Scholar
  6. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580CrossRefPubMedGoogle Scholar
  7. Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838CrossRefPubMedCentralPubMedGoogle Scholar
  8. Chehab EW, Raman G, Walley JW, Perea JV, Banu G, Theg S, Dehesh K (2006) Rice hydroperoxide lyases with unique expression patterns generate distinct aldehyde signatures in Arabidopsis. Plant Physiol 141:121–134CrossRefPubMedCentralPubMedGoogle Scholar
  9. Chen MS (2008) Inducible direct plant defence against insect herbivores: a review. Insect Sci 15:101–114CrossRefGoogle Scholar
  10. Chen H, Michael JS, Qian Q, Chen F (2012) Genetic, molecular and genomic basis of rice defense against insects. Crit Rev Plant Sci 31(1):74–91CrossRefGoogle Scholar
  11. Christensen SA, Nemchenko A, Borrego E, Murray I, Sobhy IS, Bosak L, DeBlasio S, Erb M, Robert CAM, Vaughn KA, Herrfurth C, Tumlinson J, Feussner I, Jackson D, Turlings TCJ, Engelberth J, Nansen C, Meeley R, Kolomiets MV (2013) The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J 74(1):59–73CrossRefPubMedGoogle Scholar
  12. Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–216CrossRefPubMedGoogle Scholar
  13. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A 101:1781–1785CrossRefPubMedCentralPubMedGoogle Scholar
  14. Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–734CrossRefPubMedGoogle Scholar
  15. Gomi K, Yamasaki Y, Yamamoto H, Akimitsu K (2003) Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in Citrus. Plant Physiol 160:1219–1231CrossRefGoogle Scholar
  16. Gomi K, Satoh M, Ozawa R, Shinonaga Y, Sanada S, Sasaki K, Matsumura M, Ohashi Y, Kanno H, Akimitsu K, Takabayashi J (2010) Role of hydroperoxide lyase in white-backed planthopper (Sogatella furcifera Horváth)-induced resistance to bacterial blight in rice. Plant J 61:46–57CrossRefPubMedGoogle Scholar
  17. Halitschke R, Ziegler J, Keinänen M, Baldwin IT (2004) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuate. Plant J 40:35–46CrossRefPubMedGoogle Scholar
  18. Heil M, Silva BJC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A 104:5467–5472CrossRefPubMedCentralPubMedGoogle Scholar
  19. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  20. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91CrossRefPubMedGoogle Scholar
  21. Kiritani K (1979) Pest management in rice. Ann Rev Entomol 24:279–312CrossRefGoogle Scholar
  22. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102CrossRefPubMedGoogle Scholar
  23. Liu XQ, Li F, Tang JY, Wang WH, Zhang FX, Wang GD, Chu JF, Yan CY, Wang TQ, Chu CC, Li CY (2012) Activation of the jasmonic acid pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk between the HPL and AOS branches of the oxylipin pathway in rice. PLoS ONE 7(11):e50089. doi: 10.1371/journal.pone. 0050089 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9(3):274–280CrossRefPubMedGoogle Scholar
  25. Qi JF, Zhou GX, Yang LJ, Erb M, Lu YH, Sun XL, Cheng JA, Lou YG (2011) The chloroplast-localized phospholipases D α4 and α5 regulate herbivore-induced direct and indirect defenses in rice. Plant Physiol 157:1987–1999CrossRefPubMedCentralPubMedGoogle Scholar
  26. Reymond P, Bodenhausen N, Van Poecke RM, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16(11):3132–3147CrossRefPubMedCentralPubMedGoogle Scholar
  27. Rubia-Sanchez E, Suzuki Y, Arimura K, Miyamoto K, Matsumura M, Watanabe T (2003) Comparing Nilaparvata lugens (Stål) and Sogatella furcifera (Horvath) (Homoptera: Delphacidae) feeding effects on rice plant growth processes at the vegetative stage. Crop Prot 22:967–974CrossRefGoogle Scholar
  28. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32(7):1085–1098CrossRefPubMedGoogle Scholar
  29. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci U S A 103:16672–16676CrossRefPubMedCentralPubMedGoogle Scholar
  30. Tong XH, Qi JF, Zhu XD, Mao BZ, Zeng LJ, Wang BH, Li Q, Zhou GX, Xu XJ, Lou YG, He ZH (2012) The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J 71:763–775CrossRefPubMedGoogle Scholar
  31. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plant leads to an increase in aphid performance. Proc Natl Acad Sci U S A 98:8139–8144CrossRefPubMedCentralPubMedGoogle Scholar
  32. Wei JN, Kang L (2011) Roles of (Z)-3-hexenol in plant–insect interactions. Plant Signal Behav 6(3):369–371CrossRefPubMedCentralPubMedGoogle Scholar
  33. Wu JQ, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122CrossRefPubMedCentralPubMedGoogle Scholar
  34. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Manila, pp 61–64Google Scholar
  35. Zeringue HJ (1992) Effects of C6–C10 alkenals and alkanals on eliciting a defense response in the developing cotton boll. Phytochemistry 31:2305–2308CrossRefGoogle Scholar
  36. Zhou GX, Qi JF, Ren N, Cheng JA, Erb M, Mao BZ, Lou YG (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Baohui Wang
    • 1
  • Guoxin Zhou
    • 1
  • Zhaojun Xin
    • 1
  • Rui Ji
    • 1
  • Yonggen Lou
    • 1
  1. 1.State Key Laboratory of Rice Biology, Institute of Insect ScienceZhejiang UniversityHangzhouChina

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