scholarly journals Identification of Plant Virus Receptor Candidates in the Stylets of Their Aphid Vectors

2018 ◽  
Vol 92 (14) ◽  
Author(s):  
Craig G. Webster ◽  
Elodie Pichon ◽  
Manuella van Munster ◽  
Baptiste Monsion ◽  
Maëlle Deshoux ◽  
...  

ABSTRACTPlant viruses transmitted by insects cause tremendous losses in most important crops around the world. The identification of receptors of plant viruses within their insect vectors is a key challenge to understanding the mechanisms of transmission and offers an avenue for future alternative control strategies to limit viral spread. We here report the identification of two cuticular proteins within aphid mouthparts, and we provide experimental support for the role of one of them in the transmission of a noncirculative virus. These two proteins, named Stylin-01 and Stylin-02, belong to the RR-1 cuticular protein subfamily and are highly conserved among aphid species. Using an immunolabeling approach, they were localized in the maxillary stylets of the pea aphidAcyrthosiphon pisumand the green peach aphidMyzus persicae, in the acrostyle, an organ earlier shown to harbor receptors of a noncirculative virus. A peptide motif present at the C termini of both Stylin-01 and Stylin-02 is readily accessible all over the surface of the acrostyle. Competition forin vitrobinding to the acrostyle was observed between an antibody targeting this peptide and the helper component protein P2 ofCauliflower mosaic virus. Furthermore, silencing thestylin-01but notstylin-02gene through RNA interference decreased the efficiency ofCauliflower mosaic virustransmission byMyzus persicae. These results identify the first cuticular proteins ever reported within arthropod mouthparts and distinguish Stylin-01 as the best candidate receptor for the aphid transmission of noncirculative plant viruses.IMPORTANCEMost noncirculative plant viruses transmitted by insect vectors bind to their mouthparts. They are acquired and inoculated within seconds when insects hop from plant to plant. The receptors involved remain totally elusive due to a long-standing technical bottleneck in working with insect cuticle. Here we characterize the role of the two first cuticular proteins ever identified in arthropod mouthparts. A domain of these proteins is directly accessible at the surface of the cuticle of the acrostyle, an organ at the tip of aphid stylets. The acrostyle has been shown to bind a plant virus, and we consistently demonstrated that one of the identified proteins is involved in viral transmission. Our findings provide an approach to identify proteins in insect mouthparts and point at an unprecedented gene candidate for a plant virus receptor.

2015 ◽  
Vol 89 (24) ◽  
pp. 12427-12440 ◽  
Author(s):  
Robyn Roberts ◽  
Jincan Zhang ◽  
Laura K. Mayberry ◽  
Satyanarayana Tatineni ◽  
Karen S. Browning ◽  
...  

ABSTRACTSeveral plant viruses encode elements at the 5′ end of their RNAs, which, unlike most cellular mRNAs, can initiate translation in the absence of a 5′ m7GpppG cap. Here, we describe an exceptionally long (739-nucleotide [nt]) leader sequence in triticum mosaic virus (TriMV), a recently emerged wheat pathogen that belongs to thePotyviridaefamily of positive-strand RNA viruses. We demonstrate that the TriMV 5′ leader drives strong cap-independent translation in both wheat germ extract and oat protoplasts through a novel, noncanonical translation mechanism. Translation preferentially initiates at the 13th start codon within the leader sequence independently of eIF4E but involves eIF4G. We truncated the 5′ leader to a 300-nucleotide sequence that drives cap-independent translation from the 5′ end. We show that within this sequence, translation activity relies on a stem-loop structure identified at nucleotide positions 469 to 490. The disruption of the stem significantly impairs the function of the 5′ untranslated region (UTR) in driving translation and competing against a capped RNA. Additionally, the TriMV 5′ UTR can direct translation from an internal position of a bicistronic mRNA, and unlike cap-driven translation, it is unimpaired when the 5′ end is blocked by a strong hairpin in a monocistronic reporter. However, the disruption of the identified stem structure eliminates such a translational advantage. Our results reveal a potent and uniquely controlled translation enhancer that may provide new insights into mechanisms of plant virus translational regulation.IMPORTANCEMany members of thePotyviridaefamily rely on their 5′ end for translation. Here, we show that the 739-nucleotide-long triticum mosaic virus 5′ leader bears a powerful translation element with features distinct from those described for other plant viruses. Despite the presence of 12 AUG start codons within the TriMV 5′ UTR, translation initiates primarily at the 13th AUG codon. The TriMV 5′ UTR is capable of driving cap-independent translationin vitroandin vivo, is independent of eIF4E, and can drive internal translation initiation. A hairpin structure at nucleotide positions 469 to 490 is required for the cap-independent translation and internal translation initiation abilities of the element and plays a role in the ability of the TriMV UTR to compete against a capped RNAin vitro. Our results reveal a novel translation enhancer that may provide new insights into the large diversity of plant virus translation mechanisms.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Rebeca Cuesta ◽  
Carmen Yuste-Calvo ◽  
David Gil-Cartón ◽  
Flora Sánchez ◽  
Fernando Ponz ◽  
...  

Abstract Turnip mosaic virus (TuMV), a potyvirus, is a flexible filamentous plant virus that displays a helical arrangement of coat protein copies (CPs) bound to the ssRNA genome. TuMV is a bona fide representative of the Potyvirus genus, one of most abundant groups of plant viruses, which displays a very wide host range. We have studied by cryoEM the structure of TuMV virions and its viral-like particles (VLPs) to explore the role of the interactions between proteins and RNA in the assembly of the virions. The results show that the CP-RNA interaction is needed for the correct orientation of the CP N-terminal arm, a region that plays as a molecular staple between CP subunits in the fully assembled virion.


2019 ◽  
Vol 93 (23) ◽  
Author(s):  
Alberto Cobos ◽  
Nuria Montes ◽  
Marisa López-Herranz ◽  
Miriam Gil-Valle ◽  
Israel Pagán

ABSTRACT Although vertical transmission from parents to offspring through seeds is an important fitness component of many plant viruses, very little is known about the factors affecting this process. Viruses reach the seed by direct invasion of the embryo and/or by infection of the ovules or the pollen. Thus, it can be expected that the efficiency of seed transmission would be determined by (i) virus within-host multiplication and movement, (ii) the ability of the virus to invade gametic tissues, (iii) plant seed production upon infection, and (iv) seed survival in the presence of the virus. However, these predictions have seldom been experimentally tested. To address this question, we challenged 18 Arabidopsis thaliana accessions with Turnip mosaic virus and Cucumber mosaic virus. Using these plant-virus interactions, we analyzed the relationship between the effect of virus infection on rosette and inflorescence weights; short-, medium-, and long-term seed survival; virulence; the number of seeds produced per plant; virus within-host speed of movement; virus accumulation in the rosette and inflorescence; and efficiency of seed transmission measured as a percentage and as the total number of infected seeds. Our results indicate that the best estimators of percent seed transmission are the within-host speed of movement and multiplication in the inflorescence. Together with these two infection traits, virulence and the number of seeds produced per infected plant were also associated with the number of infected seeds. Our results provide support for theoretical predictions and contribute to an understanding of the determinants of a process central to plant-virus interactions. IMPORTANCE One of the major factors contributing to plant virus long-distance dispersal is the global trade of seeds. This is because more than 25% of plant viruses can infect seeds, which are the main mode of germplasm exchange/storage, and start new epidemics in areas where they were not previously present. Despite the relevance of this process for virus epidemiology and disease emergence, the infection traits associated with the efficiency of virus seed transmission are largely unknown. Using turnip mosaic and cucumber mosaic viruses and their natural host Arabidopsis thaliana as model systems, we have identified the within-host speed of virus colonization and multiplication in the reproductive structures as the main determinants of the efficiency of seed transmission. These results contribute to shedding light on the mechanisms by which plant viruses disperse and optimize their fitness and may help in the design of more-efficient strategies to prevent seed infection.


2017 ◽  
Vol 30 (8) ◽  
pp. 631-645 ◽  
Author(s):  
Ying Wen Huang ◽  
Chung Chi Hu ◽  
Ching Hsiu Tsai ◽  
Na Sheng Lin ◽  
Yau Heiu Hsu

Plant viruses may exhibit age-dependent tissue preference in their hosts but the underlying mechanisms are not well understood. In this study, we provide several lines of evidence to reveal the determining role of a protein of the Nicotiana benthamiana chloroplast Hsp70 (NbcpHsp70) family, NbcpHsp70-2, involved in the preference of Bamboo mosaic virus (BaMV) to infect older tissues. NbcpHsp70 family proteins were identified in complexes pulled down with BaMV replicase as the bait. Among the isoforms of NbcpHsp70, only the specific silencing of NbcpHsp70-2 resulted in the significant decrease of BaMV RNA in N. benthamiana protopalsts, indicating that NbcpHsp70-2 is involved in the efficient replication of BaMV RNA. We further identified the age-dependent import regulation signal contained in the transit peptide of NbcpHsp70-2. Deletion, overexpression, and substitution experiments revealed that the signal in the transit peptide of NbcpHsp70-2 is crucial for both the import of NbcpHsp70-2 into older chloroplasts and the preference of BaMV for infecting older leaves of N. benthamiana. Together, these data demonstrated that BaMV may exploit a cellular age-dependent transportation mechanism to target a suitable environment for viral replication.


Insects ◽  
2021 ◽  
Vol 12 (12) ◽  
pp. 1073
Author(s):  
Xiao-Tian Tang ◽  
Cecilia Tamborindeguy

Autophagy, also known as type II programmed cell death, is a cellular mechanism of “self-eating”. Autophagy plays an important role against pathogen infection in numerous organisms. Recently, it has been demonstrated that autophagy can be activated and even manipulated by plant viruses to facilitate their transmission within insect vectors. However, little is known about the role of autophagy in the interactions of insect vectors with plant bacterial pathogens. ‘Candidatus Liberibacter solanacearum’ (Lso) is a phloem-limited Gram-negative bacterium that infects crops worldwide. Two Lso haplotypes, LsoA and LsoB, are transmitted by the potato psyllid, Bactericera cockerelli and cause damaging diseases in solanaceous plants (e.g., zebra chip in potatoes). Both LsoA and LsoB are transmitted by the potato psyllid in a persistent circulative manner: they colonize and replicate within psyllid tissues. Following acquisition, the gut is the first organ Lso encounters and could be a barrier for transmission. In this study, we annotated autophagy-related genes (ATGs) from the potato psyllid transcriptome and evaluated their expression in response to Lso infection at the gut interface. In total, 19 ATGs belonging to 17 different families were identified. The comprehensive expression profile analysis revealed that the majority of the ATGs were regulated in the psyllid gut following the exposure or infection to each Lso haplotype, LsoA and LsoB, suggesting a potential role of autophagy in response to Lso at the psyllid gut interface.


Previous studies on the relationship between plant viruses and their insect vectors have been carried out which viruses which are easily mechanically transmissible and whose vectors lose their infectivity within a few hours of removal from the source of infection. This type of virus has been called (Watson and Roberts 1939) non-persistent , for it was observed that the property in which viruses of this type resemble each other, and differ from those viruses whose vectors retain their infectivity for long periods, namely, the persistent viruses. It seems that these differences must lie in the nature of the viruses themselves, for viruses of both types can be transmitted by the same vector. Sugar-beet yellows virus (Petherbridge and Stirrup 1935) seems to be a member of the persistent class, for its vector, Myzus persicae , the same insect as was used in previous work on non-persistent viruses (Watson 1936, 1938; Watson and Roberts 1939), remains infective for several days after removal from the source of infection (Roland 1939). Also it is not transmissible mechanically by any of the usual methods (Quanjer 1934, 1936). The present paper, therefore, describes some studies on the vector-virus relationships of this virus by the methods which have been used previously only on the non-persistent types.


2013 ◽  
Vol 61 (2) ◽  
pp. 161 ◽  
Author(s):  
Josh C. C. M. Van Vianen ◽  
Gary J. Houliston ◽  
John D. Fletcher ◽  
Peter B. Heenan ◽  
Hazel M. Chapman

To date, most research conducted on plant viruses has centred on agricultural systems where viruses greatly reduce economic output. Introduced viruses are globally common and there is a lack of knowledge around how they might affect natural populations. Although it has been suggested that infectious disease may have played an underestimated role in past species extinctions, there is little empirical evidence. Cook’s scurvy grass (Lepidium oleraceum Sparrm. ex G.Forst; Brassicaceae) is a threatened coastal plant endemic to New Zealand. Following the discovery of Turnip mosaic virus (TuMV) in some glasshouse cultivated specimens, we surveyed wild extant Lepidium populations on the Otago coast for TuMV while screening for two other common crop viruses. We show that TuMV is almost ubiquitous among remaining wild L. oleraceum populations on the South Island’s east coast and report the first record of L. oleraceum as a host for both Cauliflower mosaic virus and Turnip yellows virus. The high incidence of virus infection throughout the study populations may make this system one of the first examples of introduced viruses affecting the conservation of a threatened plant species.


Plant Disease ◽  
2020 ◽  
Vol 104 (3) ◽  
pp. 853-859
Author(s):  
Happyness G. Mollel ◽  
Joseph Ndunguru ◽  
Peter Sseruwagi ◽  
Titus Alicai ◽  
John Colvin ◽  
...  

Begomoviruses are plant viruses that cause major losses to many economically important crops. Although they are poorly understood, begomoviruses infecting wild plants may have an important role as reservoirs in the epidemiology of viral diseases. This study reports the discovery and genomic characterization of three novel bipartite begomoviruses from wild and cultivated African basil (Ocimum gratissimum) plants collected in Uganda, East Africa. Based on the symptoms shown by the infected plants, the names proposed for these viruses are Ocimum yellow vein virus (OcYVV), Ocimum mosaic virus (OcMV), and Ocimum golden mosaic virus (OcGMV). Genome and phylogenetic analyses suggest that DNA-A of OcGMV is mostly related to begomoviruses infecting tomato in Africa, whereas those of OcYVV and OcMV are closely related to one another and highly divergent within the Old World begomoviruses. The DNA-A of all characterized begomovirus isolates are of a recombinant nature, revealing the role of recombination in the evolution of these begomoviruses. The viruses characterized here are the first identified in O. gratissimum and the first in Ocimum spp. in the African continent and could have important epidemiological consequences for cultivated basils and other important crops. [Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license .


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