Orange Leafhopper Cicadulina bipunctata Feeding Induces Gall Formation Nitrogen Dependently and Regulates Gibberellin Signaling
Abstract
:1. Introduction
2. Results
2.1. Wallaby Ear Symptoms on Rice Seedlings
2.2. Nitrogen Requirement for Gall Formation on Rice Seedlings
2.3. Regulation of GA Signaling by C. bipunctata Feeding
3. Discussion
4. Materials and Methods
4.1. Materials and Growth Conditions
4.2. Bioassay
4.2.1. Preparation of Rice Seedlings
4.2.2. Effects of Plant Growth and Gall Induction by C. bipunctata on Rice Seedlings
4.2.3. Effects of Nutrient Deficiency on Plant Growth and Gall Induction
4.2.4. Effects of Plant Hormones on Plant Growth and Gall Induction
4.2.5. Preparation of the Samples for Quantitative Real-Time PCR
4.3. Quantitative Real-Time PCR Analysis
4.4. Statistical Analyses
4.4.1. Plant Growth
4.4.2. Gall Formation
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Wilson, M.R.; Claridge, M.F. Handbook for the identification of leafhoppers and planthoppers of rice. Handb. Identif. Leafhoppers Planthoppers Rice 1991. [Google Scholar] [CrossRef]
- Matsukura, K.; Matsumura, M.; Takeuchi, H.; Endo, N.; Tokuda, M. Distribution, host plants, and seasonal occurrence of the maize orange leafhopper, Cicadulina bipunctata (Melichar) (Homoptera: Cicadellidae), in Japan. Appl. Entomol. Zool. 2009, 44, 207–214. [Google Scholar] [CrossRef]
- Kumashiro, S.; Matsukura, K.; Ogawa, R.; Matsumura, M.; Tokuda, M. Occurrence of Cicadulina bipunctata (Hemiptera: Cicadellidae) in southwestern shikoku, Japan and comparisons of gall-inducing ability between kyushu and shikoku populations. Appl. Entomol. Zool. 2014, 49, 325–330. [Google Scholar] [CrossRef] [Green Version]
- Matsukura, K.; Matsumura, M. Cultural control of leafhopper-induced maize wallaby ear symptom in forage maize via early planting dates. Crop. Prot. 2010, 29, 1401–1405. [Google Scholar] [CrossRef]
- Maramorosch, K.; Calica, C.A.; Agati, J.A.; Pableo, G. Further studies on the maize and rice leaf galls induced by Cicadulina bipunctella. Entomol. Exp. Appl. 1961, 4. [Google Scholar] [CrossRef]
- Grylls, N.E. Leafhopper Transmission of a virus causing maize wallaby ear disease. Ann. Appl. Biol. 1975, 79, 283–296. [Google Scholar] [CrossRef] [PubMed]
- Ofori, F.A.; Francki, R.I.B. Evidence that maize wallaby ear disease is caused by an insect toxin. Ann. Appl. Biol. 1983, 103, 185–189. [Google Scholar] [CrossRef]
- Ohata, S. The occurence of maize wallaby ear disease caused by the feeding of leafhopper, Cicadulina bipunctata Melichar (Homoptera, Cicadellidae). J. Jpn. Soc. Grassl. Sci. 1993, 39, 120–123. [Google Scholar] [CrossRef]
- Matsumura, M.; Tokuda, M. A mass rearing method using rice seedlings for the maize orange leafhopper Cicadulina bipunctata (Melichar) (Homoptera: Cicadellidae) and a simple method for evaluating varietal resistance of maize to maize wallaby ear disease. Kyushu Plant Prot. Res. 2004, 50, 35–39. [Google Scholar] [CrossRef]
- Tokuda, M.; Matsumura, M. Effect of temperature on the development and reproduction of the maize orange leafhopper Cicadulina bipunctata (Melichar) (Homoptera: Cicadellidae). Appl. Entomol. Zool. 2005, 40, 213–220. [Google Scholar] [CrossRef] [Green Version]
- Matsukura, K.; Matsumura, M.; Tokuda, M. Host manipulation by the orange leafhopper Cicadulina bipunctata: Gall induction on distant leaves by dose-dependent stimulation. Naturwissenschaften 2009, 96, 1059–1066. [Google Scholar] [CrossRef] [PubMed]
- Stone, G.N.; Schönrogge, K. The adaptive significance of insect gall morphology. Trends Ecol. Evol. 2003, 18, 512–522. [Google Scholar] [CrossRef]
- Matsukura, K.; Matsumura, M.; Tokuda, M. Host feeding by an herbivore improves the performance of offspring. Evol. Biol. 2012, 39, 341–347. [Google Scholar] [CrossRef]
- Mapes, C.C.; Davies, P.J. Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytol. 2001, 151, 195–202. [Google Scholar] [CrossRef]
- Mapes, C.C.; Davies, P.J. Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurosta solidaginis. New Phytol. 2001, 151, 203–212. [Google Scholar] [CrossRef]
- Straka, J.R.; Hayward, A.R.; Emery, R.J.N. Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones. J. Plant Interact. 2010, 5, 197–203. [Google Scholar] [CrossRef]
- Dorchin, N.; Hoffmann, J.H.; Stirk, W.A.; Novak, O.; Strnad, M.; Van Staden, J. Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae. Physiol. Entomol. 2009, 34, 359–369. [Google Scholar] [CrossRef]
- Yamaguchi, H.; Tanaka, H.; Hasegawa, M.; Tokuda, M.; Asami, T.; Suzuki, Y. Phytohormones and willow gall induction by a gall-inducing sawfly. New Phytol. 2012, 196, 586–595. [Google Scholar] [CrossRef]
- Takei, M.; Yoshida, S.; Kawai, T.; Hasegawa, M.; Suzuki, Y. Adaptive significance of gall formation for a gall-inducing aphids on Japanese elm trees. J. Insect Physiol. 2015, 72, 43–51. [Google Scholar] [CrossRef]
- Tokuda, M.; Jikumaru, Y.; Matsukura, K.; Takebayashi, Y.; Kumashiro, S.; Matsumura, M.; Kamiya, Y. Phytohormones related to host plant manipulation by a gall-inducing leafhopper. PLoS ONE 2013, 8. [Google Scholar] [CrossRef] [Green Version]
- Matsukura, K.; Matsumura, M. Ecology of the maize orange leafhopper, Cicadulina bipunctata (Melichar) (Hemiptera: Cicadellidae). Jpn. Agric. Res. Q. 2013, 47, 365–369. [Google Scholar] [CrossRef] [Green Version]
- Tang, Z.; Fan, X.; Li, Q.; Feng, H.; Miller, A.J.; Shen, Q.; Xu, G. Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiol. 2012, 160, 2052–2063. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takehisa, H.; Sato, Y.; Antonio, B.A.; Nagamur, Y. Global transcriptome profile of rice root in response to essential macronutrient deficiency. Plant Signal. Behav. 2013, 8, e24409. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arata, Y.; Nagasawa-Iida, A.; Uneme, H.; Nakajima, H.; Kakimoto, T.; Sato, R. The phenylquinazoline compound S-4893 is a non-competitive cytokinin antagonist that targets Arabidopsis cytokinin receptor CRE1 and promotes root growth in Arabidopsis and rice. Plant Cell Physiol. 2010, 51, 2047–2059. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, J.; Qi, T.; Hu, Z.; Fan, X.; Zhu, L.; Iqbal, M.F.; Yin, X.; Xu, G.; Fan, X. OsNAR2.1 positively regulates drought tolerance and grain yield under drought stress conditions in rice. Front. Plant Sci. 2019, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, B.; Wang, X.M.; Ma, H.Y.; Jia, Y.; Li, X.; Dai, C.C. Effects of the fungal endophyte Phomopsis liquidambari on nitrogen uptake and metabolism in rice. Plant Growth Regul. 2014, 73, 165–179. [Google Scholar] [CrossRef]
- Sopow, S.L.; Shorthouse, J.D.; Strong, W.; Quiring, D.T. Evidence for long-distance, chemical gall induction by an insect. Ecol. Lett. 2003, 6, 102–105. [Google Scholar] [CrossRef]
- Martin, J.P. Stem Galls of Sugar-Cane Induced with Insect Extracts. Science 1942, 96, 39. [Google Scholar] [CrossRef]
- Leatherdale, D. Plant Hyperplasia Induced with a Cell-Free Insect Extract. Nature 1955, 175, 553–554. [Google Scholar] [CrossRef]
- McCalla, D.R.; Genthe, M.K.; Hovanitz, W. Chemical Nature of an Insect Gall Growth-Factor. Plant. Physiol. 1962, 37, 98–103. [Google Scholar] [CrossRef] [Green Version]
- Yasui, Y.; Ohmori, Y.; Takebayashi, Y.; Sakakibara, H.; Hirano, H.-Y. WUSCHEL-RELATED HOMEOBOX4 acts as a key regulator in early leaf development in rice. PLoS Genet. 2018, 14, e1007365. [Google Scholar] [CrossRef]
- Kumashiro, S.; Matsukura, K.; Kawaura, K.; Matsumura, M.; Ogihara, Y.; Tokuda, M. Effect of barley chromosome addition on the susceptibility of wheat to feeding by a gall-inducing leafhopper. Naturwissenschaften 2011, 98, 983–987. [Google Scholar] [CrossRef] [PubMed]
- Shindo, M.; Shimomura, K.; Yamaguchi, S.; Umehara, M. Upregulation of DWARF27 is associated with increased strigolactone levels under sulfur deficiency in rice. Plant Direct 2018, 2, e00050. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hayashi, K.I.; Neve, J.; Hirose, M.; Kuboki, A.; Shimada, Y.; Kepinski, S.; Nozaki, H. Rational design of an auxin antagonist of the SCF TIR1 auxin receptor complex. ACS Chem. Biol. 2012, 7, 590–598. [Google Scholar] [CrossRef] [PubMed]
- Miyazaki, S.; Kurisu, H.; Nakata, M.; Saikawa, Y. Identification of a Cyanidin-3-O-β-Galactoside in Gall Tissue Induced by Midges on Japanese Beech (Fagus crenata Blume). Biosci. Biotechnol. Biochem. 2020, 84, 797–799. [Google Scholar] [CrossRef] [PubMed]
- Miyazaki, S.; Jiang, K.; Kobayashi, M.; Asami, T.; Nakajima, M. Helminthosporic acid functions as an agonist for gibberellin receptor. Biosci. Biotechnol. Biochem. 2017, 81, 2152–2159. [Google Scholar] [CrossRef] [Green Version]
- Yang, W.; Yoon, J.; Choi, H.; Fan, Y.; Chen, R.; An, G. Transcriptome analysis of nitrogen-starvation-responsive genes in rice. BMC Plant Biol. 2015, 15, 31. [Google Scholar] [CrossRef] [Green Version]
- Wang, W.; Hu, B.; Yuan, D.; Liu, Y.; Che, R.; Hu, Y.; Ou, S.; Liu, Y.; Zhang, Z.; Wang, H.; et al. Expression of the nitrate transporter gene OsNRT1.1A/ OsNPF6.3 confers high yield and early maturation in rice. Plant Cell 2018, 30, 638–651. [Google Scholar] [CrossRef] [Green Version]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Miyazaki, S.; Kasahara, K.; Matsui, S.; Tokuda, M.; Saikawa, Y. Orange Leafhopper Cicadulina bipunctata Feeding Induces Gall Formation Nitrogen Dependently and Regulates Gibberellin Signaling. Plants 2020, 9, 1270. https://doi.org/10.3390/plants9101270
Miyazaki S, Kasahara K, Matsui S, Tokuda M, Saikawa Y. Orange Leafhopper Cicadulina bipunctata Feeding Induces Gall Formation Nitrogen Dependently and Regulates Gibberellin Signaling. Plants. 2020; 9(10):1270. https://doi.org/10.3390/plants9101270
Chicago/Turabian StyleMiyazaki, Sho, Keita Kasahara, Soh Matsui, Makoto Tokuda, and Yoko Saikawa. 2020. "Orange Leafhopper Cicadulina bipunctata Feeding Induces Gall Formation Nitrogen Dependently and Regulates Gibberellin Signaling" Plants 9, no. 10: 1270. https://doi.org/10.3390/plants9101270