scholarly journals Silencing an E3 Ubiquitin Ligase Gene OsJMJ715 Enhances the Resistance of Rice to a Piercing-Sucking Herbivore by Activating ABA and JA Signaling Pathways

2021 ◽  
Vol 22 (23) ◽  
pp. 13020
Author(s):  
Yuebai Zhang ◽  
Mengting Chen ◽  
Shuxing Zhou ◽  
Yonggen Lou ◽  
Jing Lu

The RING-type E3 ubiquitin ligases play an important role in plant growth, development, and defense responses to abiotic stresses and pathogens. However, their roles in the resistance of plants to herbivorous insects remain largely unknown. In this study, we isolated the rice gene OsJMJ715, which encodes a RING-domain containing protein, and investigated its role in rice resistance to brown planthopper (BPH, Nilaparvata lugens). OsJMJ715 is a nucleus-localized E3 ligase whose mRNA levels were upregulated by the infestation of gravid BPH females, mechanical wounding, and treatment with JA or ABA. Silencing OsJMJ715 enhanced BPH-elicited levels of ABA, JA, and JA-Ile as well as the amount of callose deposition in plants, which in turn increased the resistance of rice to BPH by reducing the feeding of BPH and the hatching rate of BPH eggs. These findings suggest that OsJMJ715 negative regulates the BPH-induced biosynthesis of ABA, JA, and JA-Ile and that BPH benefits by enhancing the expression of OsJMJ715.

2021 ◽  
Vol 22 (22) ◽  
pp. 12182
Author(s):  
Miaofen Ye ◽  
Peng Kuai ◽  
Shuting Chen ◽  
Na Lin ◽  
Meng Ye ◽  
...  

Many plant proteins with extracellular leucine-rich repeat (eLRR) domains play an important role in plant immunity. However, the role of one class of eLRR plant proteins—the simple eLRR proteins—in plant defenses against herbivores remains largely unknown. Here, we found that a simple eLRR protein OsI-BAK1 in rice localizes to the plasma membrane. Its expression was induced by mechanical wounding, the infestation of gravid females of brown planthopper (BPH) Nilaparvata lugens or white-backed planthopper Sogatella furcifera and treatment with methyl jasmonate or abscisic acid. Silencing OsI-BAK1 (ir-ibak1) in rice enhanced the BPH-induced transcript levels of three defense-related WRKY genes (OsWRKY24, OsWRKY53 and OsWRKY70) but decreased the induced levels of ethylene. Bioassays revealed that the hatching rate was significantly lower in BPH eggs laid on ir-ibak1 plants than wild-type (WT) plants; moreover, gravid BPH females preferred to oviposit on WT plants over ir-ibak1 plants. The exogenous application of ethephon on ir-ibak1 plants eliminated the BPH oviposition preference between WT and ir-ibak1 plants but had no effect on the hatching rate of BPH eggs. These findings suggest that OsI-BAK1 acts as a negative modulator of defense responses in rice to BPH and that BPH might exploit this modulator for its own benefit.


2021 ◽  
Vol 11 ◽  
Author(s):  
Jianmei Fu ◽  
Yu Shi ◽  
Lu Wang ◽  
Hao Zhang ◽  
Jing Li ◽  
...  

The small brown planthopper (Laodelphax striatellus; SBPH) is a piercing-sucking insect that secretes salivary proteins into its plant host during feeding. However, the mechanisms by which these salivary proteins regulate plant defense responses remain poorly understood. Here, we identified the disulfide isomerase (LsPDI1) in the SBPH salivary proteome. LsPDI1 was highly expressed in the SBPH salivary glands and secreted into rice plants during feeding. Transient in planta LsPDI1 expression in the absence of signal peptide induced reactive oxygen species (ROS) burst, cell death, callose deposition, and jasmonic acid (JA) signaling pathway. Deletion mutant analysis revealed that either the a-b-b’ or the b-b’-a’ domains in LsPDI1 are required to induce cell death in plants. LsPDI1 and its orthologs were highly conserved among various planthopper species and strongly induced ROS burst and cell death in plants. Transient in Nicotiana benthamiana LsPDI1 expression impaired the performance of Spodoptera frugiperda and Myzus persicae on host plants. Hence, LsPDI1 is an important salivary elicitor that enhances plant resistance to insects by inducing the calcium, ROS, and JA signaling pathways. The findings of this study provide novel insights into the molecular mechanisms underlying plant-insect interactions.


2019 ◽  
Vol 20 (12) ◽  
pp. 3023 ◽  
Author(s):  
Zhou ◽  
Chen ◽  
Zhang ◽  
Gao ◽  
Noman ◽  
...  

Plants undergo several but very precise molecular, physiological, and biochemical modulations in response to biotic stresses. Mitogen-activated protein kinase (MAPK) cascades orchestrate multiple cellular processes including plant growth and development as well as plant responses against abiotic and biotic stresses. However, the role of MAPK kinases (MAPKKs/MKKs/MEKs) in the regulation of plant resistance to herbivores has not been extensively investigated. Here, we cloned a rice MKK gene, OsMKK3, and investigated its function. It was observed that mechanical wounding, infestation of brown planthopper (BPH) Nilaparvata lugens, and treatment with methyl jasmonate (MeJA) or salicylic acid (SA) could induce the expression of OsMKK3. The over-expression of OsMKK3 (oe-MKK3) increased levels of jasmonic acid (JA), jasmonoyl-L-isoleucine (JA-Ile), and abscisic acid (ABA), and decreased SA levels in rice after BPH attack. Additionally, the preference for feeding and oviposition, the hatching rate of BPH eggs, and BPH nymph survival rate were significantly compromised due to over-expression of OsMKK3. Besides, oe-MKK3 also augmented chlorophyll content but impaired plant growth. We confirm that MKK3 plays a pivotal role in the signaling pathway. It is proposed that OsMKK3 mediated positive regulation of rice resistance to BPH by means of herbivory-induced phytohormone dynamics.


2018 ◽  
Vol 19 (9) ◽  
pp. 2744 ◽  
Author(s):  
Lin Chen ◽  
Tiantian Cao ◽  
Jin Zhang ◽  
Yonggen Lou

Gibberellins (GAs) play pivotal roles in plant growth and development, and in defenses against pathogens. Thus far, how the GA-mediated signaling pathway regulates plant defenses against herbivores remains largely unknown. In this study, we cloned the rice GA receptor gene OsGID1, whose expression was induced by damage from the brown planthopper (BPH) Niaparvata lugens, mechanical wounding, and treatment with salicylic acid (SA), but not jasmonic acid. The overexpression of OsGID1 (oe-GID1) decreased BPH-induced levels of SA, H2O2, and three SA-pathway-related WRKY transcripts, but enhanced BPH-induced levels of ethylene. Bioassays in the laboratory revealed that gravid BPH females preferred to feed and lay eggs on wild type (WT) plants than on oe-GID1 plants. Moreover, the hatching rate of BPH eggs on oe-GID1 plants was significantly lower than that on WT plants. In the field, population densities of BPH adults and nymphs were consistently and significantly lower on oe-OsGID1 plants than on WT plants. The increased resistance in oe-GID1 plants was probably due to the increased lignin level mediated by the GA pathway, and to the decrease in the expression of the three WRKY genes. Our findings illustrated that the OsGID1-mediated GA pathway plays a positive role in mediating the resistance of rice to BPH.


Plants ◽  
2020 ◽  
Vol 9 (11) ◽  
pp. 1529
Author(s):  
Lin Chen ◽  
Peng Kuai ◽  
Miaofen Ye ◽  
Shuxing Zhou ◽  
Jing Lu ◽  
...  

The pentose phosphate pathway (PPP) plays an important role in plant growth and development, and plant responses to biotic and abiotic stresses. Yet, whether the PPP regulates plant defenses against herbivorous insects remains unclear. In this study, we cloned a rice cytosolic 6-phosphogluconate dehydrogenase gene, Os6PGDH1, which encodes the key enzyme catalyzing the third step in the reaction involving the oxidative phase of the PPP, and explored its role in rice defenses induced by brown planthopper (BPH) Nilaparvata lugens. Levels of Os6PGDH1 transcripts were detected in all five examined tissues, with the highest in outer leaf sheaths and lowest in inner leaf sheaths. Os6PGDH1 expression was strongly induced by mechanical wounding, infestation of gravid BPH females, and jasmonic acid (JA) treatment. Overexpressing Os6PGDH1 (oe6PGDH) decreased the height of rice plants and the mass of the aboveground part of plants, but slightly increased the length of plant roots. In addition, the overexpression of Os6PGDH1 enhanced levels of BPH-induced JA, jasmonoyl-isoleucine (JA-Ile), and H2O2, but decreased BPH-induced levels of ethylene. Bioassays revealed that gravid BPH females preferred to feed and lay eggs on wild-type (WT) plants over oe6PGDH plants; moreover, the hatching rate of BPH eggs raised on oe6PGDH plants and the fecundity of BPH females fed on these were significantly lower than the eggs and the females raised and fed on WT plants. Taken together, these results indicate that Os6PGDH1 plays a pivotal role not only in rice growth but also in the resistance of rice to BPH by modulating JA, ethylene, and H2O2 pathways.


2019 ◽  
Vol 86 (4) ◽  
Author(s):  
Tong-Pu Li ◽  
Chun-Ying Zhou ◽  
Si-Si Zha ◽  
Jun-Tao Gong ◽  
Zhiyong Xi ◽  
...  

ABSTRACT The brown planthopper Nilaparvata lugens (Hemiptera) is a major pest of rice crops in Asia. Artificial transinfections of Wolbachia have recently been used for reducing host impacts, but transinfections have not yet been undertaken with another important endosymbiont, Cardinium. This endosymbiont can manipulate the reproduction of hosts through phenotypes such as cytoplasmic incompatibility (CI), which is strong in the related white-backed planthopper, Sogatella furcifera (Hemiptera). Here, we stably infected N. lugens with Cardinium from S. furcifera and showed that it exhibits perfect maternal transmission in N. lugens. The density of Cardinium varied across developmental stages and tissues of the transinfected host. Cardinium did not induce strong CI in N. lugens, likely due to its low density in testicles. The infection did decrease fecundity and hatching rate in the transinfected host, but a decrease in fecundity was not apparent when transinfected females mated with Wolbachia-infected males. The experiments show the feasibility of transferring Cardinium endosymbionts across hosts, but the deleterious effects of Cardinium on N. lugens limit its potential to spread in wild populations of N. lugens in the absence of strong CI. IMPORTANCE In this study we established a Cardinium-infected N. lugens line that possessed complete maternal transmission. Cardinium had a widespread distribution in tissues of N. lugens, and this infection decreased the fecundity and hatching rate of the host. Our findings emphasize the feasibility of transinfection of Cardinium in insects, which expands the range of endosymbionts that could be manipulated for pest control.


Insects ◽  
2019 ◽  
Vol 10 (2) ◽  
pp. 57
Author(s):  
Xu Ding ◽  
Xi Huang ◽  
Litong Sun ◽  
Jincai Wu ◽  
Jinglan Liu

Fluridone (FLU) was a pyrrolidone herbicide that was used for selective weeding in wheat, rice, corn and pasture and was also a biosynthesis inhibitor of abscisic acid (ABA), a significant plant hormone. ABA-promoted callose deposition facilitates rice resistance to pests but whether FLU had the opposite influence was unknown. The effects of FLU on the feeding behavior of the brown planthopper (Nilaparvata lugens Stål; BPH), after feeding with rice plants treated with FLU, were studied, using an electrical penetration graph (EPG). For susceptible rice cultivar (TN1), the duration for which BPH sucked phloem sap (N4 wave duration) after 15 μmol/L of FLU treatment was longer than that of the control but decreased after 30 and 60 μmol/L FLU treatments. Fecundity of BPH treated with 15 μmol/L FLU had no significant change, while the deposition area of callose was significantly decreased. For moderately-resistant rice cultivar (IR42), no differences in BPH feeding behavior and fecundity were observed but the deposition area of callose declined after treated with 15 μmol/L of FLU. These findings suggested that a low concentration of FLU (15 μmol/L) promoted BPH feeding behavior in TN1 but not in IR42 and the response in IR42 appeared to be more complicated, which provided supplementary evidence that ABA promoted plant resistance to BPH.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Satyabrata Nanda ◽  
San-Yue Yuan ◽  
Feng-Xia Lai ◽  
Wei-Xia Wang ◽  
Qiang Fu ◽  
...  

Abstract Rice production and sustainability are challenged by its most dreadful pest, the brown planthopper (Nilaparvata lugens Stål, BPH). Therefore, the studies on rice-BPH interactions and their underlying mechanisms are of high interest. The rice ontogenetic defense, such as the role of microRNAs (miRNAs) has mostly been investigated against the pathogens, with only a few reports existing against the insect infestations. Thus, revealing the involvement of rice miRNAs in response to BPH infestations will be beneficial in understanding these complex interactions. In this study, the small RNA profiling of the IR56 rice in response to separate BPH infestations of varied virulence levels identified the BPH-responsive miRNAs and revealed the differential transcript abundance of several miRNAs during a compatible and incompatible rice-BPH interaction. The miRNA sequence analysis identified 218 known and 28 novel miRNAs distributed in 54 miRNA families. Additionally, 138 and 140 numbers of differentially expressed (DE) miRNAs were identified during the compatible and incompatible interaction, respectively. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis revealed the target gene candidates of DE miRNAs (including osa-miR2871a-3p, osa-miR172a, osa-miR166a-5p, osa-miR2120, and osa-miR1859) that might be involved in the IR56 rice defense responses against BPH infestation. Conversely, osa-miR530-5p, osa-miR812s, osa-miR2118g, osa-miR156l-5p, osa-miR435 and two of the novel miRNAs, including novel_16 and novel_52 might negatively modulate the IR56 rice defense. The expressional validation of the selected miRNAs and their targets further supported the IR56 rice defense regulatory network. Based on our results, we have proposed a conceptual model depicting the miRNA defense regulatory network in the IR56 rice against BPH infestation. The findings from the study add further insights into the molecular mechanisms of rice-BPH interactions and will be helpful for the future researches.


2021 ◽  
Vol 12 ◽  
Author(s):  
Xiao-Xiao Shi ◽  
Mu-Fei Zhu ◽  
Ni Wang ◽  
Yuan-Jie Huang ◽  
Min-Jing Zhang ◽  
...  

Ceramides are bioactive sphingolipids that have been implicated in insect development; however, their role in insect reproduction remains poorly understood. Here, we report the pivotal role of neutral ceramidase (NCER) in the female reproduction of the brown planthopper (BPH), Nilaparvata lugens (Stål), a significant pest in rice cultivation in Asia. LC-MS/MS demonstrated that, among different developmental stages of BPH, the levels of ceramides were highest in 1st instar nymphs and lowest in adults. The transcription of NCER was negatively correlated with the levels of ceramides at different developmental stages of BPH, in that the transcript levels of NCER were the highest, whereas ceramides levels were the lowest in BPH adults. Knocking down NCER through RNA interference (RNAi) increased the levels of ceramides in BPH females and ovaries, which resulted in a delay in oocyte maturation, a reduction in oviposition and egg hatching rate, as well as the production of vulnerable offspring. Transmission electron microscopy (TEM) analysis and TdT-mediated dUTP Nick-End Labeling (TUNEL) assays showed mitochondrial deficiency and apoptosis in NCER-deficient oocytes. Taken together, these results suggest that NCER plays a crucial role in female reproduction in BPH, likely by regulating the levels of ceramides.


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