**Plant Virus Emergence**

Editors

**Michael Goodin Jeanmarie Verchot**

MDPI • Basel • Beijing • Wuhan • Barcelona • Belgrade • Manchester • Tokyo • Cluj • Tianjin

*Editors* Michael Goodin University of Kentucky USA

Jeanmarie Verchot Texas A&M University USA

*Editorial Office* MDPI St. Alban-Anlage 66 4052 Basel, Switzerland

This is a reprint of articles from the Special Issue published online in the open access journal *Viruses* (ISSN 1999-4915) (available at: https://www.mdpi.com/journal/viruses/special issues/ emergence).

For citation purposes, cite each article independently as indicated on the article page online and as indicated below:

LastName, A.A.; LastName, B.B.; LastName, C.C. Article Title. *Journal Name* **Year**, *Volume Number*, Page Range.

**ISBN 978-3-0365-0596-1 (Hbk) ISBN 978-3-0365-0597-8 (PDF)**

Cover image courtesy of Michael Goodin and Jeanmarie Verchot.

© 2021 by the authors. Articles in this book are Open Access and distributed under the Creative Commons Attribution (CC BY) license, which allows users to download, copy and build upon published articles, as long as the author and publisher are properly credited, which ensures maximum dissemination and a wider impact of our publications.

The book as a whole is distributed by MDPI under the terms and conditions of the Creative Commons license CC BY-NC-ND.

## **Contents**


## **Przemysław Wieczorek, Marta Budziszewska, Patryk Frąckowiak and Aleksandra Obrępalska-Stęplowska** Development of a New Tomato Torrado Virus-Based Vector Tagged with GFP for Monitoring Virus Movement in Plants Reprinted from: *Viruses* **2020**, *12*, 1195, doi:10.3390/v12101195 .................... **137 Zacharie LeBlanc, Peter Waterhouse and Julia Bally**


## **About the Editors**

**Michael Goodin** is a distinguished plant virologist who was a Professor of Plant Pathology at the University of Kentucky, in Lexington, Kentucky. Michael was born in Jamaica. He was an undergraduate at Brock University in Canada, where he received degrees in both Biology and Chemistry in 1989. He received his M.Sc. and then Ph.D. at Pennsylvania State University, where he trained with C. P. Romaine in plant pathology. He was a postdoctoral fellow with Andy Jackson at the University of California, Berkeley, from 1996 to 2002 and has been a faculty member in the Department of Plant Pathology at the University of Kentucky since 2002. His strong research record includes the development of tools for the in planta study of plant–virus interactions that are now used worldwide. He contributed significantly to the generation of the first functional mini-replicon system for a negative-strand plant RNA virus, the sonchus yellow net virus. Michael pioneered the discovery of emerging viruses infecting coffee plants in Brazil. In 2018, he was awarded the title of the American Society for Microbiology Honorary Diversity Lecturer in recognition of his scholarship, research, and creativity.

**Jeanmarie Verchot** is a Professor in the Department of Plant Pathology & Microbiology and a Fellow of the Institute for Plant Genomics and Biotechnology at Texas A&M University. Jeanmarie was born in New Jersey, USA. She was an undergraduate at Rutgers University, Cook College, in New Jersey and received a degree in genetics in 1987. She received her Ph.D. from Texas A&M University, where she trained with James C. Carrington in microbiology. She was a postdoctoral fellow with David Baulcombe at the Sainsbury Laboratory in the UK from 1996 to 1998. She was a faculty member at Oklahoma State University from 1998 to 2017. She was a Director for the Texas A&M Agrilife Center in Dallas from 2017–2019, then became a fellow of the Institute for Plant Genomics and Biotechnology at Texas A&M University. She is a Professor of Plant Pathology at Texas A&M University. Her strong research record includes uncovering mechanisms for potato virus X cell-to-cell movement, describing the mechanisms for plasmodiophorid vectors to transmit viruses to plant roots, the discovery of new virus genomes in canna lily, the development of a reverse genetic system for rose rosette virus, and detailing the mechanism for potexvirus interaction with the endomembrane system and the role of the unfolded protein response in monitoring potyvirus and potexvirus infection.

## *Editorial* **Introduction to Special Issue of Plant Virus Emergence**

**Michael Goodin 1,\*,† and Jeanmarie Verchot 2,\***


Academic Editor: K. Andrew White Received: 24 December 2020; Accepted: 30 December 2020; Published: 1 January 2021

We are pleased to present in this Special Issue a series of reviews and research studies on the topic of "*Plant Virus Emergence*". The issue includes a series of articles that elaborate on important plant virus diseases that are among the most recent epidemiological concerns. This Special Issue is predicated on the paradigm that plant virus epidemiology, outbreaks, epidemics, and pandemics parallel zoonotic viruses, and can be consequential to global food security [1]. There is evidence that local, regional, national, and global trade of agricultural products has aided the global dispersal of plant virus diseases. Expanding farmlands into pristine natural areas has created opportunities for viruses in native landscapes to invade crops, while the movement of food and food products disseminates viruses creating epidemics or pandemics [2,3]. As covered in several of the submissions, a number of factors drive plant virus emergence. Included in these are direct anthropomorphic activities, reviewed in "*Homo sapiens: the superspreader of plant viral diseases*" [4]. This theme of distribution of cultivated plants around the world, dispersed from their centers of domestication, implicates humans as being responsible for the novel encounters between plants and their pests. Alternatively, in the article "*Disease Pandemics and Major Epidemics Arising from New Encounters between Indigenous Viruses and Introduced Crops Viruses*" [5], Jones considers the phenomenon of spillover, the movement of viruses from non-cultivated vegetation into introduced crop plants. Such a phenomenon parallels that which occurred in the emergence of Ebola [6], Hendra, and Nipah viruses [7]. Climate change has also created favorable environments for insects that vector plant viruses. Regulatory agencies around the globe are working together to prevent or mitigate the introduction of plant viruses into new areas where they can cause devastation to food security. Moreover, plant virus outbreaks not only directly impact food supply, they also incidentally affect human health.

Other articles in this Special Issue describe plant viruses that are studied for their associations with "outbreak" phenomena (sudden appearance), reservoir hosts and "spillover" phenomena (transfer from wild to domesticated areas), common genetics, and reliance on "vectors" for viral spread. In "*Potato virus Y emergence and evolution from the Andes of South America to become a major destructive pathogen of potato and other solanaceous crops worldwide*", Torrance and Talianksly [8] discuss how PVY emerged from the Andes of South America to become a worldwide threat to potato and other solanaceous crops. Due to its broad host range and recombination between strains, PVY and related potyviruses show an episodic emergence of new strains with new virulences. Torrance and Talianksly make the case for research that integrates phylogenetic analyses and high-throughput next-generation sequencing for the detection, identification, and surveillance of new virus strains. Along these lines, Herath et al. present, in "*Family Level Phylogenies Reveal Relationships of Plant Viruses within the Order Bunyavirales*" [9], the importance of phylogenetics in consideration of emergence negative-sense segmented RNA viruses infecting arthropods, protozoans, plants, animals, and humans. Comprehensive phylogenetic analyses of the four "hallmark"

genes demonstrated the relatedness of virus species across host eukaryotic species, herein reinforcing the similar emergence phenomena that occur in both plant and animal systems. Furthermore, for these viruses, the link between plants and animals is made by the vectors of the plant-infecting viruses.

Insects are significant drivers of virus emergence, as featured in submissions by Pinheiro-Lima et al., "*Transmission of the Bean-Associated Cytorhabdovirus by the Whitefly Bemisia tabaci MEAM1*" [10], and Schoeny, et al., "*Can Winged Aphid Abundance Be a Predictor of Cucurbit Aphid-Borne Yellows Virus Epidemics in Melon Crop?*" [11]. These studies confirm that we must avoid dogmatic perspectives on plant virus transmission, as the first demonstration of a whitefly-transmitted rhabdovirus. Heretofore unknown virus–vector combinations should be anticipated as drivers of future outbreaks, as demonstrated for *Bemisia tabaci* Middle East-Asia Minor 1 (MEAM1) transmission of bean-associated cytorhabdovirus to common bean, and with a lower efficiency to cowpea and soybean. However, not only is the particular vector important, but the timing of its occurrence in fields relative to crop age can influence emergence. For example, the abundance of *A. gossypii* during the first two weeks after planting is a good predictor of disease caused by CABYV. Early control of the vector is necessary to minimize the potential for CABYV epidemics in melon crops.

Increasingly, scientists depend upon advanced DNA and RNA sequencing technologies to monitor the emergence and spread of new plant virus strains or species, facilitate novel virus discovery, and uncover the etiology of complex diseases. In the article by Weiland et al., "*RNAseq Analysis of Rhizomania-Infected Sugar Beet Provides the First Genome Sequence of Beet Necrotic Yellow Vein Virus from the USA and Identifies a Novel Alphanecrovirus and Putative Satellite Viruses*" [12], advanced sequencing technology was used to discover a complex of viruses underlying rhizomania of sugarbeet. Historically, BNYVV is the acknowledged primary cause of rhizomania however, this work demonstrates the impact on disease severity of co-infecting viruses like beet soil-borne mosaic virus (BSBMV), beet soil-borne virus (BSBV), beet black scorch virus (BBSV), and beet virus Q (BVQ), and a novel Alphanecrovirus.

SARS-CoV-2 is the third coronavirus to emerge in recent years, SARS and MERS being the other two, suggesting that virus surveillance and discovery in reservoir species is important preparatory work for modeling disease outbreaks and planning for vaccines before their emergence in humans. The discovery of emergent virus species and strains requires further molecular characterization. Moodley et al., in "*Emergence and Full Genome Analysis of Tomato Torrado Virus in South Africa*" [13], report new virus genome sequences for ToTV. Wieczorek et al., in "*Development of a New Tomato Torrado Virus-Based Vector Tagged with GFP for Monitoring Virus Movement in Plants*" [14] produce infectious clones needed to study virus infection and molecular interactions with the hosts. Such infectious clone technology is foundational in understanding virus molecular functions, as well as in developing plant viral-based protein expression vectors. It is in this arena that scientists employ plant-based protein expression systems for plant-based vaccine and pharmaceutical production. Developing plant-made antivirals and vaccines is essential to contain and mitigate outbreaks at their earliest outset, thus mitigating recurrences of the tragic events related to the SARS-CoV-2/COVID-19 pandemic. LeBlanc et al. [15] review the state-of-the-art systems for producing "mammalian-compatible" biomolecules in plants, particularly as related to glycosylation.

We hope that you find the collection in this Special Issue informative and of interest. As the public becomes informed of scientific theories on virus disease emergence and spread during the COVID-19 pandemic, it is timely that plant viruses are included in the discussion. We hope that the articles in this Special Issue on "*Plant Virus Emergence*" highlight elaborate efforts in plant virology that support broad models for virus outbreaks, spillovers, genetics, reliance on "vectors" and human trade for spread, as well as the maintenance of viruses in "reservoir" hosts. In closing, we thank all of the authors for their enlightening contributions to this Special Issue.

**Funding:** This work was supported by a grant from NSF (IOS #1759034).

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


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© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

## *Editorial* **In Tribute to Michael Goodin**

#### **Jeanmarie Verchot 1,\*, Andrew O. Jackson <sup>2</sup> and Anne E. Simon <sup>3</sup>**


#### Academic Editor: K. Andrew White

Received: 4 January 2021; Accepted: 6 January 2021; Published: 8 January 2021

It is with great sadness and sympathy for his family and the plant virology community that we convey the passing of Michael Goodin unexpectedly in December 2020. Michael contributed enormously as co-editor of this special issue on *Emerging Plant Viruses* for MDPI-Viruses; hence, we wish to dedicate this issue to his memory. We are calling this issue a passion project in memory of Michael, because, if you ever had the honor to work with him or interact with him at a study section or conference, you know of his exuberance and passion for plant virology. Michael's well-respected research focused mainly on plant-infecting rhabdoviruses and the biochemistry and cell biology of virus/host interactions during infection. His love for coffee led to his recent work with coffee ringspot viruses, which are emerging threats to coffee production and quality. But Michael was much more than an accomplished scientist. He had a special passion for his family, friends, and colleagues. He was passionate about photography and public and science education. He enjoyed travel, particularly in national and state parks, as well as abroad, as illustrated by his outstanding photographs. Michael loved to talk about growing up in Jamaica and the deliciousness of Jamaican cuisine; he even brought goat to cook an unforgettable, authentic Caribbean meal after giving an invited seminar at the University of Maryland!

Dr. Michael Goodin (1967–2020)

Michael obtained a PhD in 1995 from Pennsylvania State University in Pete Romaine's lab. There, he generated a productive thesis that investigated the virus-induced La France disease in cultivated mushrooms. He then spent five years working as a postdoc in Andy Jackson's lab at UC-Berkeley. Michael obtained a faculty position in the Plant Pathology Department at the University of Kentucky in 2002, and was a professor and the Director of the Plant Science Biological Imaging Facility.

In summary, Michael was a wonderful friend and colleague to so many, and an enthusiastic supporter of plant virology. He was vibrant, creative, and a passionate lover of life. We hope that when you read this special issue, and the letter from Michael, you share with us the memory of his desire to spread the word about emerging viruses that can impact the foods we eat (and drink). We hope that those of you who knew Michael Goodin will reflect on his research contributions to plant virology, the sense of community he instilled amongst us, and his inspiration to students and colleagues, and smile when remembering his laughter and joy at conferences.

Thank you Michael, for all that you have done. You will be greatly missed.

**Conflicts of Interest:** The authors declare no conflict of interest.

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
