Abstract
The plant ROP/RAC protein belongs to a subfamily of Rho family GTPases that inimitably exists in plants. It is considered an all-powerful molecular switch that modulates various plant developmental processes and plant defense responses to multifarious stresses. However, their exact roles are currently not entirely clear. Herein, the role of GhRac6, a ROP/RAC member from Gossypium hirsutum, was explored in the plant defense response to aphid feeding using transgenic technology. The deduced sequence of the GhRac6 protein is highly homologous to that of ROP/RAC proteins from other plants. GhRac6 expression was significantly upregulated in cotton leaves after damage by cotton aphids or wounding. The results of choice and no-choice tests showed that the number of aphids on GhRac6-overexpressing transgenic Arabidopsis was more than that on wild-type plants, while the secreted quantity of aphid honeydew in transgenic Arabidopsis was less than that in wild-type plants. Furthermore, the soluble sugar content and the proline content were higher in transgenic than in wild-type Arabidopsis to a certain extent. The activity of PAL and CAT in transgenic Arabidopsis was also higher than that in wild-type plants. Callose deposits were more abundant in transgenic than in wild-type Arabidopsis. The expression of related defense genes in the salicylic acid signaling pathway was considerably higher in transgenic than in wild-type Arabidopsis. These results collectively demonstrated that the cotton ROP gene GhRac6 improved the plant defense response to aphid feeding by regulating some aphid resistance indexes.
Similar content being viewed by others
Abbreviations
- SSH:
-
Suppression subtractive hybridization 62
- qPCR:
-
Quantitative real-time polymerase chain reaction
- EST:
-
Expressed sequence tag
- ORF:
-
Open reading frame
- MS:
-
Murashige and Skoog
- PCR:
-
Polymerase chain reaction
- PAL:
-
Phenylalanine ammonia lyase
- CAT:
-
Catalase
References
Asprodites N (2005) The cloning and characterization of two ROP/RAC G-proteins from Gossypium Hirsutum. Uni of New Orleans Theses and Dissertations. 233
Chen JJ, Wang XF (2000) Plant physiol Exp guide. China Agriculture Press, Beijing (in Chinese)
Chen L, Shiotani K, Togashi T, Miki D, Aoyama M, Wong HL, Shimamoto K (2010) Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance. Plant Cell Physiol 51:585–595
Delmer DP, Pear JR, Andrawis A, Stalker DM (1995) Genes encoding small GTP-binding proteins analogous to mammalian rac are preferentially expressed in developing cotton fibers. Mol Gen Genet 248:43–51
Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci 93:6025–6030
Duan CX, Peng GS, Wang XM, Zhu ZD (2013) Differences in the physiological response of resistant and susceptible rice varieties infested by the small brown planthopper. Chin J Appl Entomol 50:145–153
Feiguelman G, Fu Y, Yalovsky S (2018) ROP GTPases structure-function and signaling pathways. Plant Physiol 176:57–79
Gu Y, Wang Z, Yang Z (2004) ROP/RAC GTPase: an old new master regulator for plant signaling. Curr Opin Plant Biol 7:527–536
Hoefle C, Huesmann C, Schultheiss H, Börnke F, Hensel G, Kumlehn J, Hückelhoven R (2011) A barley ROP GTPase activating protein associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23:2422–2439
Jin L, Mackey DM (2017) Measuring callose deposition, an indicator of cell wall reinforcement, during bacterial infection in Arabidopsis. In: Plant Pattern Recognition Receptors: Methods and Protocols. pp 195–205
Kaloshian I, Walling LL (2005) Hemipterans as plant pathogens. Annu Rev Phytopathol 43:491–521
Kawano Y, Kaneko-Kawano T, Shimamoto K (2014) Rho family GTPase-dependent immunity in plants and animals. Front Plant Sci 5:1–12
Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proc Natl Acad Sci 96:10922–10926
Kim DS, Hwang BK (2014) An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J Exp Bot 65:2295–2306
Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019
Kim HJ, Triplett BA (2004) Characterization of GhRac1 GTPase expressed in developing cotton (Gossypium hirsutum L.) fibers. BBA Gene Struct Expr 1679:214–221
Li TT, Jiang WZ, Gu TT, Liu YY, Xu JP, Liu GJ, Cao CX (2016) Relationship between aphid-resistance and leaf nutrient content of cucumber. Shandong Agricul Sci 48:44–47 50
Luo L, Yang YZ, Yang Z, Li CR, Zhang JM (2017) Identification of the genes involved in cotton induced defense to attack of cotton aphids (Aphis gossypii). J Biobased Mater Bio 11:379–384
Mao H, Zhu HH, Han JQ (2017) Wheat ROP proteins modulate defense response through lignin metabolism. Plant Sci 262:32–38
Mitchell C, Brennan RM, Graham J, Karley AJ (2016) Plant defense against herbivorous pests: exploiting resistance and tolerance traits for sustainable crop protection. Front Plant Sci 7:1–8
Mony FTZ, Ali MS, Islam MN, Choudhury S, Hossain MS (2017) Effect of salicylic acid and varieties on incidence of aphid and yield of mustard (Doctoral dissertation)
Mou S, Liu Z, Gao F, Yang S, Su M, Shen L, He S (2017) CaHDZ27, a homeodomain-leucine zipper I protein, positively regulates the resistance to Ralstonia solanacearum infection in pepper. Mol Plant-Microbe Interact 30:960–973
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nibau C, Wu H, Cheung AY (2006) RAC/ROP GTPases: ‘hubs’ for signal integration and diversification in plants. Trends Plant Sci 11:309–315
Nisbet AJ, Woodford JAT, Strang RHC (1994) Quantifying aphid feeding on non-radioactive food sources. Entomol Exp Appl 72:85–89
Pandey GK, Sharma M, Pandey A, Shanmugam T Emerging (2015) Roles of Rho GTPases in plants//GTPases. Springer International Publishing. pp 45–55
Qiu A, Liu Z, Li J, Chen Y, Guan D, He S (2016) The ectopic expression of CaRop1 modulates the response of tobacco plants to Ralstonia solanacearum and aphids. Front Plant Sci 7:1–13
Rasool B, McGowan J, Pastok D, Marcus SE, Morris J, Verrall SR, Foyer CH (2017) Redox control of aphid resistance through altered cell wall composition and nutritional quality. Plant Physiol 1–37
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:320–324
Schwartzberg EG, Tumlinson JH (2014) Aphid honeydew alters plant defence responses. Funct Ecol 28:386–394
Sharma I, Ahmad P (2014) Catalase: a versatile antioxidant in plants. Oxidative Damage to Plants. pp 131–148
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20
Winge P, Brembu T, Kristensen R, Bones AM (2000) Genetic structure and evolution of RAC-GTPases in Arabidopsis thaliana. Genetics 156:1959–1971
Zhang JM, Ma LF, Li W, Zhang J, Li DD, Li XB (2014) Cotton TCTP1 gene encoding a translationally controlled tumor protein participates in plant response and tolerance to aphids. Plant Cell Tissue Organ Cult 117:145–156
Zhou FC, Ren J, Chen XH, Yang AM, Hu QJ, Zhang JJ, He J (2014) The effects of Aphis gossypii sucking on the antibiotic substance in cucumber leaves. J Yangzhou Uni 35:99–103
Züst T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:1–19
Funding
This work was supported by a grant from the National Natural Science Foundation of China (Grant No. 31471783).
Author information
Authors and Affiliations
Contributions
Z.J.M. and Y.Y.Z. designed the research. Y.Z., L.L., L.J.J., Y.S., and Z.G.H. performed the experiments. Y.Z., Z.J.M., and W.X.P. analyzed the data and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yang, Z., Liu, J., Luo, L. et al. The Cotton GhRac6 Gene Encoding a Plant ROP/RAC Protein Improves the Plant Defense Response to Aphid Feeding. Plant Mol Biol Rep 36, 888–896 (2018). https://doi.org/10.1007/s11105-018-1127-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-018-1127-6