Genetic and biochemical mechanisms of rice resistance to planthopper

Key message

This article presents a comprehensive review on the genetic and biochemicalmechanisms governing rice-planthopper interactions, aiming to contribute substantialplanthopper control and facilitate breeding for resistance to planthoppers in rice.

Abstract

The rice planthopper is the most destructive pest of rice and a substantial threat to rice production. The brown planthopper (BPH), white-backed planthopper (WBPH) and small brown planthopper (SBPH) are three species of delphacid planthoppers and important piercing-sucking pests of rice. Host-plant resistance has been recognized as the most practical, economical and environmentally friendly strategy to control planthoppers. Until now, at least 30, 14 and 34 major genes/quantitative trait loci for resistance to BPH, WBPH and SBPH have been identified, respectively. Recent inheritance and molecular mapping of gene analysis showed that some planthopper-resistance genes in rice derived from different donors aggregate in clusters, while resistance to these three species of planthoppers in a single donor is governed not by any one dominant gene but by multiple genes. Notably, Bph14, Bph26, Bph3 and Bph29 were successfully identified as BPH-resistance genes in rice. Biological and chemical studies on the feeding of planthoppers indicate that rice plants have acquired various forms of defence against planthoppers. Between the rice-planthopper interactions, rice plants defend against planthoppers through activation the salicylic acid-dependent systemic acquired resistance but not jasmonate-dependent hormone response pathways. Transgenic rice for the planthopper-resistance mechanism shows that jasmonate and its metabolites function diversely in rice’s resistance to planthopper. Understanding the genetic and biochemical mechanisms underlying resistance in rice will contribute to the substantial control of such pests and facilitate breeding for rice’s resistance to planthopper more efficiently.

     

The complete mitochondrial genome sequence of Sogatella furcifera (Horváth) and a comparative mitogenomic analysis of three predominant rice planthoppers

The white-backed planthopper (WBPH), Sogatella furcifera (Horváth), is one of the most destructive pests of rice crops in many Asian countries. Using long-PCR and shotgun library methods, we sequenced the entire mitochondrial genomes (mt-genomes) of two WBPH individuals. Total lengths of the mt-genome of the two WBPH individuals were 16,612 bp and 16,654 bp with an identical AT content of 76.19%. Among the 13 protein coding genes (PCGs), only nad5 used an atypical initiation codon GTG. Most of the tRNA genes had the typical cloverleaf secondary structure except that the dihydrouridine (DHU) arms in two trnS genes and the TΨC arm of trnG gene did not form a stable stem-loop structure. Similar to the brown planthopper (BPH), Nilaparvata lugens (Stål), and the small brown planthopper (SBPH), Laodelphax striatellus (Fallén), some extraordinary features were observed in the WBPH mt-genome. These include similar gene rearrangement pattern, unusually short length of the atp8 gene and variable numbers of tandem repeat (VNTR) structure in control region. Interestingly, the same tandem repeat unit with stable secondary structure appeared in two different planthoppers, WBPH and SBPH, which belong to two different genera of the Delphacidae. This peculiar feature provides a direct evidence for the close relationship between the two planthoppers and updates our understanding of the evolutionary characteristics of mitochondrial control region. Comparison with two other predominant rice planthoppers (BPH and SBPH) revealed that different PCGs of mitochondria exhibit different evolutionary patterns.     

稻飞虱迁飞种群的上灯行为节律研究

【目的】明确稻飞虱迁飞种群的上灯行为节律,以指导其大田迁入种群和迁出种群的发生预测与灾变预警。【方法】本研究运用逐时自动灯诱装置对2010和2011连续两年稻飞虱迁飞种群的上灯行为节律进行了系统研究。【结果】灰飞虱Laodelphax striatellus迁飞种群上灯始见期和灯诱虫量年际间差异不明显,白背飞虱Sogatella furcifera和褐飞虱Nilaparvata lugens迁飞过境种群上灯始见期和灯诱虫量年际间差异较大。此外,灰飞虱迁飞种群的特大高峰期和高峰期逐时灯诱虫量百分比与一般上灯期和零星上灯期相比突出了晨暮双峰型中的暮峰型上灯行为特点;白背飞虱迁飞种群特大高峰期逐时灯诱虫量百分比与高峰期和一般期相比突出了晨暮双峰型中的晨峰型生物学特性。【结论】稻飞虱迁飞种群的上灯行为节律存在种的特异性,这一行为节律除了受环境因素的影响外主要与其生物学特性有关。     

稻飞虱翅型纯系后代个体的翅型分化对光周期变化不敏感

【目的】为了明确光周期和遗传因子在稻飞虱翅型分化中的作用, 研究了3种稻飞虱（褐飞虱Nilaparvata lugens、白背飞虱Sogatella furcifera和灰飞虱Laodelphax striatellus）翅型纯系或近纯系在不同光照时数下的翅型分化比率。【方法】以经过5~45代连续翅型筛选后的褐飞虱、白背飞虱和灰飞虱的长翅型和短翅型纯系或近纯系为材料, 在室内分别测定了其在长光照（16和20 h）、短光照(4~12 h)和正常光照(14 h) 3类光周期条件下饲养后, 雌、雄成虫中长翅和短翅个体出现的比率及存活率。【结果】白背飞虱和灰飞虱的长翅型纯系M♂×M♀或短翅型纯系B♂×B♀在不同光周期下的翅型比率均无显著差异（P>0.05）。褐飞虱短翅型近纯系B♂×B♀的雌虫短翅率和成虫总短翅率在不同光周期下也无显著差异（P>0.05）, 但雄虫短翅率在正常光照14 h和短光照4 h下显著高于长光照20 h下的（P<0.05）。当褐飞虱短翅型达到纯系后, 其后代翅型在6~16 h光照条件下无显著差异。褐飞虱长翅型近纯系M♂×M♀的后代虽有短翅个体出现, 但是雌虫和雄虫的各自短翅率在不同光周期下无显著差异（P>0.05), 仅总体短翅率在12 h光照条件下的显著高于16 h下的（P<0.05）。褐飞虱长、短翅型杂交筛选品系M♂×B♀的雌虫短翅率随光照时数的延长而升高; 灰飞虱杂交筛选品系M♂×B♀的短翅雄虫随光照时数的缩短而增多（P<0.05）, 但当筛选代次达到45代时, 这种趋势不再显著。3种稻飞虱长翅型和短翅型纯系或近纯系若虫的存活率会稍低于长、短翅型杂交后代的存活率, 但长、短翅型品系的存活率在6~16 h光照条件下差异不显著(P>0.05)。【结论】稻飞虱翅型分化对光周期的反应受飞虱本身遗传背景的影响, 翅型纯系后代个体的翅型分化对光周期变化不敏感。     

Two whitebacked planthopper resistance genes in rice share the same loci with those for brown planthopper resistance

The whitebacked planthopper (WBPH), Sogatella furcifera, and brown planthopper (BPH) Nilaparvata lugens St?l are important sucking insects of rice (Oryza sativa L.) crops throughout the world. Rice 'B5', which has derived its resistance genes from the wild rice O. officinalis Wall ex Watt, is a line that is highly resistant to both WBPH and BPH. Previously, two resistance genes against BPH, Qbp1, and Qbp2 in 'B5' had been mapped onto chromosome 3 and chromosome 4, respectively. In this study, we employed a mapping population composed of 187 recombinant inbred lines (RILs), produced from a cross between 'B5' and susceptible variety 'Minghui63', to locate the WBPH and BPH resistance genes. A RFLP survey of the bulked extremes from the RIL population identified two genomic regions, one on chromosome 3 and the other on chromosome 4, likely containing the resistance genes to planthoppers. QTL analysis of the RILs further confirmed that two WBPH resistance genes were mapped on the same loci as Qbp1 and Qbp2, using a linkage map with 242 molecular markers distributed on 12 rice chromosomes. Of the two WBPH resistance genes, one designated Wbph7(t) was located within a 1.1-cM region between R1925 and G1318 on chromosome 3, the other designated Wbph8(t) was within a 0.3-cM region flanked by R288 and S11182 on chromosome 4. A two-way analysis of variance showed that two loci acted independently with each other in determining WBPH resistance. The results have significant implications in studying the interactions between sucking insects and plants and in breeding programs of resistance to rice planthoppers.     

水稻飞虱的抗药性监测研究

1989-1993年选用有机磷、氨基甲酸酯和拟除虫菊酯三大粪12种常用杀虫剂,对水稻褐飞虱和白背飞虱进行了5年系统的抗药性监测研究,发现两种飞虱对药剂的敏感性年度间变化较大,分析可能与其迁飞习性有关。将我们所测的LD50与日本Nagata(1967)测定结果比较．褐飞虱对有机磷类的抗性倍数为3.22-16．12倍,对氨基甲酸酯类为5．59-9．12倍;白背飞虱对有机磷类的抗性为48．90-208.16倍．对氨基甲酸酯类为3．29-19．50倍．抗性发展速率明显高于褐飞虱。两种飞虱对菊酯类药剂的敏感性差异较大。抗马拉硫磷的褐飞虱种群对二氯苯醚菊酯表现较高交互抗性。     

稻虱缨小蜂对褐飞虱和白背飞虱卵的识别机制

研究了室内条件下信息化合物及稻飞虱卵的形态特征在稻虱缨小蜂识别2种卵寄主褐飞虱和白背飞虱中的作用。结果表明,褐飞虱和白背飞虱雌成虫诱导的水稻挥发物对稻虱缨小蜂的引诱作用无显著差异,各自的引诱比例(头数)分别为57.50%(23头)和42.50%(17头)。稻虱缨小蜂对2种飞虱4组材料,完整卵、磨碎卵、带卵叶鞘和若虫为害叶鞘的行为反应,除了在褐飞虱完整卵上的搜索时间极显著地长于在白背飞虱完整卵上的以外,其余的均不存在差异。挥发物捕集结果表明,褐飞虱和白背飞虱雌成虫诱导的水稻挥发物组成相非常一致。上述结果表明水稻挥发物、稻飞虱利它素及飞虱卵的形态特征在稻虱缨小蜂识别褐飞虱和白背飞虱卵中的作用不明显。文中就稻虱缨小蜂识别2种寄主的机制进行了讨论。     

稻飞虱种群发生的调查与取样技术

稻飞虱是中国和许多国家水稻生产上的主要害虫,属r对策暴发危害类型。其中,褐飞虱和白背飞虱是典型的远距离迁飞性害虫,具有大区域同期"突增"和"突减"的灾变特性;灰飞虱则主要以本地越冬为主,远距离迁飞对种群结构的影响较小,但其传播的病毒病对水稻生产的影响更甚。针对3种稻飞虱的生物学特性,本文发展了稻飞虱田间种群发生与危害等的调查与取样技术,为其种群发生及其监测预警提供技术支撑。     

QUANTIFYING PREDATION BY UMMELIATA INSEC-TICEPS BOES. ET STR. (ARANEAE: LINYPHIIDAE) ON RICE PLANTHOPPERS USING ELISA*

Abstract An enzyme-linked immunosorbent assay (ELISA) has been developed to quantify predation by Ummeliata insecticeps Boes. et Str. on rice planthoppers in paddy fields in Dasha Township, Guangdong Province. The assay was completely specific for rice planthopper materials. The detection periods for antigens after an adult of U. insecticeps had fed on three 3–5th instar nymphs of white-back planthopper (WBPH), Sogatella furcifera (Horvath), and brown planthopper (BPH), Nilaparvata lugens (Stal), at room temperature were 96 h and 120 h, respectively. The proportion of individual species of predators scoring positive ranged from 19. 05% to 47. 34% for WBPH, and from 9. 25% to 66. 67% for BPH in the early rice season. Although the numbers of the rice planthoppers consumed by U. insecticeps increased with increasing prey densities, the predation rates declined. When rice planthopper densities were low, the predation rates were relatively high. This kind of predation can explain why the rice planthoppers have never reached outbreak levels in rice fields in Dasha Township since 1973.     

褐飞虱和白背飞虱的取食为害对水稻营养生长的影响

对塑料钵栽培的水稻进行罩宠试验,研究了褐飞虱和白背飞虱在不同若虫密度下取食为害对水稻营养生长的影响．结果表明,两种飞虱的成虫干重、水稻叶面积和其地上部干重因若虫密度的增加而下降．叶片干重占地上部干重的比例和稻株分配给叶片干物质量随为害程度的加重而增大;褐飞虱和白背飞虱总干重（X）与稻株地上部损失量（Y）之间存在着极显著的线性关系．两种飞虱干重每增加1mg,水稻地上部干重则分别损失26.01mg和21．90mg．讨论了稻飞虱取食为害对水稻致害的可能机制．     

2020年江苏省稻飞虱虫源地及暴发成因分析

为了明确江苏省稻飞虱(白背飞虱Sogatella furcifera Horváth和褐飞虱Nilaparvata lugens St?l)在沉寂近10年后再次暴发的成因,通过分析江苏2020年白背飞虱和褐飞虱的田间调查及灯诱数据,并结合气象条件,研究了江苏省稻飞虱暴发的主要影响因素。结果表明：(1)2020年,江苏省白背飞虱虫源主要来自于江西中、北部,湖南东部以及湖北东部;褐飞虱虫源主要来自于安徽南部、浙江北部、本省南部以及江西省中北部。(2)江淮地区自6月中旬至7月下旬的超长降雨期有利于江苏省早期迁入虫源大量降落。(3)9月初,田间已存在大量褐飞虱短翅型成虫,适宜的秋季温度促使田间短翅型褐飞虱大量繁殖,导致后期田间褐飞虱大暴发。总而言之,超长降雨期有利于早期稻飞虱的迁入降落,而秋季的适宜温度引发短翅型成虫大量繁殖,是导致江苏省稻飞虱在沉寂近10年后再次暴发的主要因素。这些结果为稻飞虱暴发规律的阐明及可持续治理提供了理论依据和参考价值。     

用ELISA方法定量评价食虫沟瘤蛛对稻飞虱的捕食作用(英文)

对捕食性节肢动物的捕食作用进行评价是害虫生物防治研究的一个重要内容。本文利用酶联免疫吸附试验（ＥＬＩＳＡ）定量评价了食虫沟瘤蛛对稻飞虱的捕食作用。结果表明,方法特异性完全符合试验要求;食虫沟瘤蛛在捕食３头３－５龄白背飞虱或褐飞虱若虫后的检出期分别为９６小时和１２０小时;在早稻田中,捕食性天敌对白背飞虱和褐飞虱的阳性反应率分别为１９．０５％－４７．３４％和１９．０５％－６６．６７％,在飞虱密度较低时,捕食性天敌仍表现出较高的阳性率;捕食量随飞虱密度的增加而增加,但捕食率下降。捕食性节肢动物是调节褐飞虱种群动态的重要因子之一。     

Role of hydroperoxide lyase in white-backed planthopper (Sogatella furcifera Horváth)-induced resistance to bacterial blight in rice, Oryza sativa L.

A pre-infestation of the white-backed planthopper (WBPH), Sogatella furcifera Horváth, conferred resistance to bacterial blight caused by Xanthomonas oryzae pv. oryzae ( Xoo ) in rice ( Oryza sativa  L.) under both laboratory and field conditions. The infestation of another planthopper species, the brown planthopper (BPH) Nilaparvata lugens Stål, did not significantly reduce the incidence of bacterial blight symptoms. A large-scale screening using a rice DNA microarray and quantitative RT-PCR revealed that WBPH infestation caused the upregulation of more defence-related genes than did BPH infestation. Hydroperoxide lyase 2 ( OsHPL2 ), an enzyme for producing C₆ volatiles, was upregulated by WBPH infestation, but not by BPH infestation. One C₆ volatile, ( E )-2-hexenal, accumulated in rice after WBPH infestation, but not after BPH infestation. A direct application of ( E )-2-hexenal to a liquid culture of Xoo inhibited the growth of the bacterium. Furthermore, a vapour treatment of rice plants with ( E )-2-hexenal induced resistance to bacterial blight. OsHPL2 -overexpressing transgenic rice plants exhibited increased resistance to bacterial blight. Based on these data, we conclude that OsHPL2 and its derived ( E )-2-hexenal play some role in WBPH-induced resistance in rice.     

Parasitism of Brown Planthopper and Whitebacked Planthopper by Agamermis unka in Korea

Adults of the brown planthopper (BPH) and the whitebacked planthopper (WBPH) that migrated into Korea from China were not parasitized by the mermithid, Agamermis unka. BPH and WBPH collected from Korean rice fields were parasitized. Parasitism of BPH in the lst-3rd, 4th, and 5th instars, and adults was 31.5%, 61.5%, 66.4%, and 45.5%, respectively, whereas parasitism of the same stages of WBPH was 50%, 50%, 100% and 90.7%, respectively. Parasitism of BPH by A. unka significantly reduced the number of eggs. Only 4.2% of the parasitized females contained eggs, whereas 85.6% of unparasitized females had eggs. Tilling of rice fields significantly increased mermithid parasitism of BPH. Mermithids parasitized 39.3% of caged adults in the untilled field and 77.8% in the tilled field.     

Pyramided rice lines harbouring Allium sativum (asal) and Galanthus nivalis (gna) lectin genes impart enhanced resistance against major sap-sucking pests

We have developed transgene pyramided rice lines, endowed with enhanced resistance to major sap-sucking insects, through sexual crosses made between two stable transgenic rice lines containing Allium sativum (asal) and Galanthus nivalis (gna) lectin genes. Presence and expression of asal and gna genes in pyramided lines were confirmed by PCR and western blot analyses. Segregation analysis of F₂ progenies disclosed digenic (9:3:3:1) inheritance of the transgenes. Homozygous F₃ plants carrying asal and gna genes were identified employing genetic and molecular methods besides insect bioassays. Pyramided lines, infested with brown planthopper (BPH), green leafhopper (GLH) and whitebacked planthopper (WBPH), proved more effective in reducing insect survival, fecundity, feeding ability besides delayed development of insects as compared to the parental transgenics. Under infested conditions, pyramided lines were found superior to the parental transgenics in their seed yield potential. This study represents first report on pyramiding of two lectin genes into rice exhibiting enhanced resistance against major sucking pests. The pyramided lines appear promising and might serve as a novel genetic resource in rice breeding aimed at durable and broad based resistance against hoppers.     

小粒野生稻导入系对稻飞虱的抗性鉴定与分析

稻飞虱是水稻生产最严重的害虫之一。野生稻拥有丰富的抗虫基因资源,导入系是鉴定和利用野生稻有利基因的有效途径。本研究通过对371份小粒野生稻导入系进行抗褐飞虱和白背飞虱接虫鉴定,分别筛选出了11份抗、72份中抗褐飞虱的材料和7份抗、45份中抗白背飞虱的材料,其中有5份材料兼抗褐飞虱和白背飞虱,这是从小粒野生稻中鉴定出抗白背飞虱材料的首次报道。通过对2份抗性导入系材料与感虫亲本杂交构建的F1和F2群体的抗虫鉴定和分析表明:K41对褐飞虱和白背飞虱的抗性受2对显性抗虫基因通过互补作用所控制;P114对褐飞虱和白背飞虱的抗性都是由1对主效的隐性基因控制。这些结果必将有利于小粒野生稻抗稻飞虱的基因定位和育种利用。     

Genetics of resistance of rice cultivar ARC10550 to Bangladesh brown pianthopper teletype

Resistance to brown planthopper in rice cultivar ARC 10550 was found to be governed by a single recessive gene which was designatedbph 5. It conveys resistance to brown planthopper populations in South Asia but not to the populations in East and Southeast Asia. This gene segregated independently of four other known genes for brown planthopper resistance. It should be possible to combine this gene with any of the other four genes to develop rice cultivars with a broad spectrum of resistance.     

Influence of rice black streaked dwarf virus on the ecological fitness of non-vector planthopper Nilaparvata lugens （Hemiptera： Delphacidae）

Rice black streak dwarf virus （RBSDV） is transmitted by the small brown planthopper （SBPH）, Laodelphax striatellus （Fallen）. Non-vector rice brown planthopper （BPH）, Nilaparvata lugens （Stal）, shares the same host rice plants with SBPH in paddy fields. The changes in nutritional composition of rice plants infected by RBSDV and the ecological fitness of BPH feeding on the infected plants were studied under both artificial climate chamber and field conditions. Contents of 16 detected amino acids and soluble sugar in RBSDV infected rice plants were higher than those in the healthy ones. On the diseased plants BPH had significantly higher nymphal survival rates, nymphal duration of the males, weight of the female adults, as well as egg hatchability compared to BPH being fed on healthy plants. However, there was no obvious difference in female nymph duration, longevity and fecundity. Defense enzymes （superoxidase dismutase, SOD and catalase, CAT） and detoxifying enzymes （carboxylesterase, CAE and glutathione S-transferase, GST） in BPH adults fed on diseased plants had markedly higher activities. The results indicate rice plants infected by RBSDV improved the ecological fitness of the brown planthopper, a serious pest but not a transmitter of the RBSDV virus.