A decade ago, the value of Nicotiana benthamiana as a tool for plant molecular biologists was beginning to be appreciated. Scientists were using it to study plant-microbe and protein-protein interactions, and it was the species of choice with which to activate plasmid-encoded viruses, screen for gene functions with virus-induced gene silencing (VIGS), and transiently express genes by leaf agroinfiltration. However, little information about the species’ origin, diversity, genetics, and genomics was available, and biologists were asking the question of whether N. benthamiana is a second fiddle or virtuoso. In this review, we look at the increased knowledge about the species and its applications over the past decade. Although N. benthamiana may still be the sidekick to Arabidopsis, it shines ever more brightly with realized and yet-to-be-exploited potential.

The Rise and Rise of Nicotiana benthamiana: A Plant for All Reasons.

Potyviruses are the largest group of plant infecting RNA viruses that cause significant losses in a wide range of crops across the globe. The majority of viruses in the genus Potyvirus are transmitted by aphids in a non-persistent, non-circulative manner and have been extensively studied vis-a-vis their structure, taxonomy, evolution, diagnosis, transmission, and molecular interactions with hosts. This comprehensive review exclusively discusses potyviruses and their transmission by aphid vectors, specifically in the light of several virus, aphid and plant factors, and how their interplay influences potyviral binding in aphids, aphid behavior and fitness, host plant biochemistry, virus epidemics, and transmission bottlenecks. We present the heatmap of the global distribution of potyvirus species, variation in the potyviral coat protein gene, and top aphid vectors of potyviruses. Lastly, we examine how the fundamental understanding of these multi-partite interactions through multi-omics approaches is already contributing to, and can have future implications for, devising effective and sustainable management strategies against aphid-transmitted potyviruses to global agriculture.

Aphid Transmission of Potyvirus: The Largest Plant-Infecting RNA Virus Genus.

Background: Nicotiana benthamiana has been widely used for transient gene expression assays and as a model plant in the study of plant-microbe interactions, lipid engineering and RNA silencing pathways. Assembling the sequence of its transcriptome provides information that, in conjunction with the genome sequence, will facilitate gaining insight into the plant's capacity for high-level transient transgene expression, generation of mobile gene silencing signals, and hyper-susceptibility to viral infection. Methodology/Results: RNA-seq libraries from 9 different tissues were deep sequenced and assembled, de novo, into a representation of the transcriptome. The assembly, of16GB of sequence, yielded 237,340 contigs, clustering into 119,014 transcripts (unigenes). Between 80 and 85% of reads from all tissues could be mapped back to the full transcriptome. Approximately 63% of the unigenes exhibited a match to the Solgenomics tomato predicted proteins database. Approximately 94% of the Solgenomics N. benthamiana unigene set (16,024 sequences) matched our unigene set (119,014 sequences). Using homology searches we identified 31 homologues that are involved in RNAi-associated pathways in Arabidopsis thaliana, and show that they possess the domains characteristic of these proteins. Of these genes, the RNA dependent RNA polymerase gene, Rdr1, is transcribed but has a 72 nt insertion in exon1 that would cause premature termination of translation. Dicer-like 3 (DCL3) appears to lack both the DEAD helicase motif and second dsRNA binding motif, and DCL2 and AGO4b have unexpectedly high levels of transcription. Conclusions: The assembled and annotated representation of the transcriptome and list of RNAi-associated sequences are accessible at www.benthgenome.com alongside a draft genome assembly. These genomic resources will be very useful for further study of the developmental, metabolic and defense pathways of N. benthamiana and in understanding the mechanisms behind the features which have made it such a well-used model plant. © 2013 Nakasugi et al.

De Novo Transcriptome Sequence Assembly and Analysis of RNA Silencing Genes of Nicotiana benthamiana

In this review, encouraged by the dictum of Theodosius Dobzhansky that “Nothing in biology makes sense except in the light of evolution”, we outline the likely evolutionary pathways that have resulted in the observed similarities and differences of the extant molecules, biology, distribution, etc. of the potyvirids and, especially, its largest genus, the potyviruses. The potyvirids are a family of plant-infecting RNA-genome viruses. They had a single polyphyletic origin, and all share at least three of their genes (i.e., the helicase region of their CI protein, the RdRp region of their NIb protein and their coat protein) with other viruses which are otherwise unrelated. Potyvirids fall into 11 genera of which the potyviruses, the largest, include more than 150 distinct viruses found worldwide. The first potyvirus probably originated 15,000–30,000 years ago, in a Eurasian grass host, by acquiring crucial changes to its coat protein and HC-Pro protein, which enabled it to be transmitted by migrating host-seeking aphids. All potyviruses are aphid-borne and, in nature, infect discreet sets of monocotyledonous or eudicotyledonous angiosperms. All potyvirus genomes are under negative selection; the HC-Pro, CP, Nia, and NIb genes are most strongly selected, and the PIPO gene least, but there are overriding virus specific differences; for example, all turnip mosaic virus genes are more strongly conserved than those of potato virus Y. Estimates of dN/dS (ω) indicate whether potyvirus populations have been evolving as one or more subpopulations and could be used to help define species boundaries. Recombinants are common in many potyvirus populations (20%–64% in five examined), but recombination seems to be an uncommon speciation mechanism as, of 149 distinct potyviruses, only two were clear recombinants. Human activities, especially trade and farming, have fostered and spread both potyviruses and their aphid vectors throughout the world, especially over the past five centuries. The world distribution of potyviruses, especially those found on islands, indicates that potyviruses may be more frequently or effectively transmitted by seed than experimental tests suggest. Only two meta-genomic potyviruses have been recorded from animal samples, and both are probably contaminants.

/pdf/the-potyviruses-an-evolutionary-synthesis-is-emerging-22pqzk5c6d.pdf

The Potyviruses: An Evolutionary Synthesis Is Emerging.

Reactive oxygen species (ROS) and reactive nitrogen species (RNS) play a pivotal role in the dynamic cell signaling systems in plants, even under biotic and abiotic stress conditions. Over the past two decades, various studies have endorsed the notion that these molecules can act as intracellular and intercellular signaling molecules at a very low concentration to control plant growth and development, symbiotic association, and defense mechanisms in response to biotic and abiotic stress conditions. However, the upsurge of ROS and RNS under stressful conditions can lead to cell damage, retarded growth, and delayed development of plants. As signaling molecules, ROS and RNS have gained great attention from plant scientists and have been studied under different developmental stages of plants. However, the role of RNS and RNS signaling in plant–microbe interactions is still unknown. Different organelles of plant cells contain the enzymes necessary for the formation of ROS and RNS as well as their scavengers, and the spatial and temporal positions of these enzymes determine the signaling pathways. In the present review, we aimed to report the production of ROS and RNS, their role as signaling molecules during plant–microbe interactions, and the antioxidant system as a balancing system in the synthesis and elimination of these species. 

/pdf/the-key-roles-of-ros-and-rns-as-a-signaling-molecule-in-3hx4oknk.pdf

The Key Roles of ROS and RNS as a Signaling Molecule in Plant–Microbe Interactions

Catharanthus mosaic virus: A potyvirus from a gymnosperm, Welwitschia mirabilis.

Isolates of an Australian indigenous virus, Yellow tailﬂower mild mottle virus (YTMMV-Kalbarri), and an exotic virus,Pelargonium zonate spot virus (PZSV-SW13), are described from Anthocercis ilicifolia subsp. ilicifolia (red-striped tail-ﬂower, family Solanaceae), a species endemic to Western Australia. This is the ﬁrst report of either virus fromthis plant species. The complete genome sequences of YTMMV-Kalbarri and of PZSV-SW13 were obtained. YTMMV-Kalbarri shared 97% nucleotide pairwise identity with the sequence of the type isolate YTMMV-Cervantes. Thesequence PZSV-SW13 shared greatest sequence identity with the partial sequence of an Australian isolate of PZSV, alsofrom a wild plant, and with a sunﬂower-derived isolate of PZSV from Argentina. An experimental host range studywas done of YTMMV-Kalbarri using cultivated and wild solanaceous and non-solanaceous plants. Most solanaceousplants became systemically infected, with symptoms of systemic infection ranging from symptomless to whole plantnecrosis. Based on these studies, it is suggested that YTMMV has the potential to become a pathogen of commercialspecies of Solanaceae. This study provides further evidence that PZSV is present in wild plants in Australia, in this casean indigenous host species, and possible routes by which it invaded Australia are discussed.Keywords: anulavirus, indigenous plant virus, plant virus ecology, tobamovirus, virus invasion, virus emergenceAnthocercis (family Solanaceae, subfamily Nicotianoi-deae) is a genus of 15 plant species endemic to southernAustralia (Haegi, 1986). Previously, a tobamovirus(genus Tobamovirus, family Virgaviridae) was isolatedfrom A. littoria (yellow tailﬂower), a spindly shrub, 3 min height, that grows along the coastline in calcareoussand, limestone ridges and sand dunes of southwesternAustralia, but the virus was not detected from A. viscosa(sticky tailﬂower) plants growing in Albany, 400 km tothe south. The new tobamovirus was named Yellow tail-ﬂower mild mottle virus (YTMMV; Wylie et al., 2014).Pelargonium zonate spot virus (PZSV; genus Anulavi-rus, family Bromoviridae) was ﬁrst isolated from Pelar-gonium zonale (Geraniaceae) in Italy (Quacquarelli G Luis-Arteaga & Cambra,2000; Gebre-Selassie et al., 2002; Finetti-Sialer & Galli-telli, 2003; Liu & Sears, 2007; Escriu et al., 2009; Gulat-i-Sakhuja et al., 2009; Lapidot et al., 2010; Blouin et al.,2013; Giolitti et al., 2014). Its geographical rangeincludes much of Europe and the Americas. In Australia,PZSV was recently described for the ﬁrst time in Cakilemaritima (Brassicaceae), a self-introduced exotic weedspecies (Luo et al., 2010).This study describes the complete genome sequences ofnew isolates of YTMMV and PZSV that co-infected a wildplant of Anthocercis ilicifolia subsp. ilicifolia (red-stripedtailﬂower), a new host species for both viruses. Althoughdetails of the host range of PZSV have been published, thepotential host range of YTMMV is not known. The natu-ral hosts of YTMMV live at the interface between wildand managed systems, and consequently the opportunityexists for the virus to expand its host range into cultivatedplant species. Thus, an experimental host range study wasundertaken of the new YTMMV isolate and the type YT-MMV isolate, and the potential of YTMMV to emerge asa pathogen of commercial importance is discussed. Fur-ther, it is speculated as to how PZSV may have enteredAustralia, given that it has not yet been detected there incommercial plantings.

/pdf/yellow-tailflower-mild-mottle-virus-and-pelargonium-zonate-3ecpqtxeuj.pdf

Yellow tailflower mild mottle virus and Pelargonium zonate spot virus co‐infect a wild plant of red‐striped tailflower in Australia

Tobamovirus is a group of viruses that have become serious pathogens of crop plants. As part of a study informing risk of wild plant virus spill over to crops, we investigated the capacity of a solanaceous-infecting tobamovirus from an isolated indigenous flora to adapt to new exotic hosts. Yellow tailflower mild mottle virus (YTMMV) (genus Tobamovirus, family Virgaviridae) was isolated from a wild plant of yellow tailflower (Anthocercis littoria, family Solanaceae) and initially passaged through a plant of Nicotiana benthamiana, then one of Nicotiana glutinosa where a single local lesion was used to inoculate a N. benthamiana plant. Sap from this plant was used as starting material for nine serial passages through three plant species. The virus titre was recorded periodically, and 85% of the virus genome was sequenced at each passage for each host. Six polymorphic sites were found in the YTMMV genome across all hosts and passages. At five of these, the alternate alleles became fixed in the viral genome until the end of the experiment. Of these five alleles, one was a non-synonymous mutation (U1499C) that occurred only when the virus replicated in tomato. The mutant isolate harbouring U1499C, designated YTMMV-δ, increased its titre over passages in tomato and outcompeted the wild-type isolate when both were co-inoculated to tomato. That YTMMV-δ had greater reproductive fitness in an exotic host than did the wild type isolate suggests YTMMV evolution is influenced by host changes.

/pdf/evolution-of-a-wild-plant-tobamovirus-passaged-through-an-3acwrbnu56.pdf

Evolution of a wild-plant tobamovirus passaged through an exotic host: Fixation of mutations and increased replication

As part of an investigation into viruses of wild plants in Australia, a contiguous sequence of 3935 nucleotides was obtained after shotgun sequencing of RNA isolated from an asymptomatic wild legume, Gompholobium preissii. Phylogenetic analysis of the sequence revealed that it most closely resembled that of Trailing lespedeza virus 1 (TLV1), a virus isolated from a wild legume in America. The proposed virus, named Gompholobium virus A, and TLV1 are genetically closest to viruses in the genera Alphacarmovirus and Pelarspovirus, family Tombusviridae, but they share features distinguishing them from both groups.

A novel member of the Tombusviridae from a wild legume, Gompholobium preissii.

The south-west Australian floristic region is one of 36 United Nations global hotspots of international species diversity Considering the high biodiversity of the flora, it is likely that the plant virus flora is also abundant and genetically diverse, although only 15 indigenous plant viruses have been described from the flora of Western Australia Colonisation of Australia by foreign powers from the 1830s onwards saw the introduction of thousands of exotic plant species and their pathogens, including plant viruses Clearance of the original flora for agriculture and housing has created interfaces between the new exotic flora of exotic crops, pastures, gardens and weeds and the remnants of the original one The actions of humans and the creation of these interfaces between ecosystems have provided opportunities for exotic viruses to interact with indigenous plants, and for indigenous viruses to interact with exotic hosts

A component of this thesis describes studies to gain a greater understanding of the identity and evolution of the plant viruses present in the indigenous flora of Western Australia and how viruses are adapting to new host opportunities A metagenomics approach was used to identify virus-like sequences from plant samples along transects that spanned interfaces between highly modified, partially modified and relatively unmodified sites 78 novel viruses were identified Most of these were from indigenous plants, and analysis of them confirmed our hypothesis that viruses of this indigenous flora are abundant, genetically diverse and largely unknown None of the viruses found in indigenous plants also occurred in the exotic plants sampled, or vice versa The exotic viruses, Catharanthus mosaic virus, barley yellow dwarf virus and white clover mosaic virus, were found in exotic plants at ecosystem interfaces, but not in indigenous plants, suggesting that viral movement across exotic-indigenous floral interfaces may not be widespread Despite these findings, the continuing invasion by exotic viruses, as evidenced by our discovery in Australia of Catharanthus mosaic virus, demonstrates the failure of quarantine practices to prevent new viruses arriving, thereby posing potential threats to indigenous plants 

An indigenous virus might extend its host range to infect exotic weeds or crop plants We used yellow tailflower mild mottle virus (YTMMV) as a model to test how an indigenous virus might interact with exotic hosts it had never encountered before YTMMV is a contact-transmissible tobamovirus isolated from endemic Anthocercis species (family Solanaceae) An isolate of YTMMV was passaged through plants of Nicotiana benthamiana, tomato and black nightshade, and its genome was sequenced after every passage to determine the presence of nonsynonymous (NS) and synonymous nucleotide substitutions Only one fixed NS nucleotide substitution was observed in the intervening region (IR) of the viral genome, and it occurred only in tomato The passages through tomato were repeated, and a different single NS substitution occurred adjacent to the NS substitution that occurred in the first passage experiment This finding suggested that NS substitutions in the IR of YTMMV were being selected in tomato

Tobamovirus virions are famously stable under a range of treatments An assessment of the durability of YTMMV virions under different treatments such as time under different temperature regimes, incubation in milk solution and sodium hydroxide was done YTMMV was shown to be more resilient to inactivation using these treatments than related viruses, tobacco mosaic virus and green cucumber mild mosaic virus The study into transmissibility and longevity of virions of YTMMV is a pre-emptive study that will be applicable should YTMMV spill over into crops 

The study of plant virus biodiversity in the wild and at the interface of ecosystems will increase our understanding of how viruses influence ecosystems, particularly on resilience to biotic and abiotic stress tolerance, longevity and fecundity The potential application of such knowledge to agriculture is important, but it is as yet unacknowledged because of the dearth of examples A far greater research effort is needed to understand the roles viruses play in ecosystems and the molecular mechanisms by which these are achieved These areas are where in-depth studies of wild plant-virus interactions will have their greatest impact

Virosphere in flux: Old and new viruses in an ancient land

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