Plant viruses may be reshaping our world

July 17, 2019

The community of viruses is staggeringly vast. Occupying every conceivable biological niche, from searing undersea vents to frigid tundra, these enigmatic invaders, hovering between inert matter and life, circumnavigate the globe in the hundreds of trillions. They are the most abundant life forms on Earth.

Viruses are justly feared as ingenious pathogens, causing diseases in everything they invade, including virtually all bacteria, fungi, plants and animals. Recent advances in the field of virology, however, suggest that viruses play a more significant and complex role than previously appreciated and may be essential to the functioning of diverse ecosystems. The viral world constitutes the most abundant life form on Earth. The graphic illustrates the staggering amount of genetic material contained in viruses. Graphic by Shireen Dooling Download Full Image

We now know that humans contain roughly 100,000 pieces of viral DNA elements, which make up around 8% of our genome. Speculation on the role of these ancient viral fragments ranges from protection against disease to increasing the risk of cancer or other serious illnesses, though researchers acknowledge they have barely scratched the surface of this enigma.

A new review article appearing in the journal Nature Reviews Microbiology highlights the evolution and ecology of plant viruses. Arvind Varsani, a researcher at ASU’s Biodesign Institute, joins an international team to explore many details of viral dynamics. They describe the subtle interplay between three components of the viral infection process: the virus itself, the plant cell hosts infected by the virus and the vectors that act as go-betweens — an intricate system evolving over some 450 million years. All three elements are embedded within wider relations of the surrounding ecosystem. 

Recent studies in the field of virology have shown that viruses are sometimes beneficial to the organisms they infect. “Prior to this people have always seen viruses as disease-causing entities,” Varsani said. “This breaks all the dogmas of how we study viruses. We have a section where we review mutualism and symbiosis and also how some of the symbiotic relationships are being uncoupled.”

Virologist Arvind Varsani is a researcher in the Biodesign Center for Fundamental and Applied Microbiomics, the Center for Mechanisms of Evolution and ASU's School of Life Sciences.

Elusive wanderer

In 1892, Russian botanist Dmitri Ivanovsky conducted a simple experiment that would have momentous implications for science and medicine. He collected sap from a diseased tobacco plant, fed the substance through very fine pores and showed that this filtered fluid could infect a healthy tobacco plant. The filtering ensured that whatever the disease-causing entity was, it was tinier than a bacterium. (Dutch plant specialist and microbiologist Martinus Beijerinck dubbed the mysterious pathogenic substance a virus, though its true form — invisible to light microscopy — only appeared in 1931, with the invention of the electron microscope.) A rod-shaped plant invader, known as tobacco mosaic virus, had revealed itself — the first virus on record. Since this time, thousands of distinct species have been identified, yet they represent a tiny fraction of the viral universe, most of which remains unexplored.

Indeed, even the question of what constitutes a virus has no single answer. Their sizes vary enormously, from a virus like Ebola, carrying a tiny handful of genes, to recently discovered giant viruses. Rivaling some bacteria in size, giant viruses can carry elements of the machinery required for translation, throwing their status as nonliving entities into question.

“The way I look at viruses now is from a philosophical angle,” Varsani said. “They are a dynamic entity and they have multiple lifestyles, ranging from basic, where the virus is fully reliant on the host for replication, to some cases where it’s only partly reliant on the host.”

Because some viruses can evolve so rapidly, trading and acquiring new genetic elements, their genomes can become chimeric or even fragmented, making their proper classification a serious challenge for the field of virology.

From the standpoint of ecology, plant viruses are particularly important for a number of reasons. Plants make up over 80% of the biomass on Earth, exerting a greater impact on the planet’s diverse ecosystems than viruses infecting other kingdoms of life. Plant viruses have obvious importance for food crops and ornamental plants, and a range of viruses are responsible for an estimated $60 billion in crop losses worldwide each year.

To capture the astonishing richness of the planet’s viral universe, researchers have gone beyond early methods of pinpointing individual virus particles and analyzing them. Techniques of metaviromics are used to probe environments for the full panoply of viruses they contain. The method, which relies on piecing together multiple DNA or RNA genomes from environmental samples, has been recently used to identify vast numbers of previously undocumented viruses. In the case of plant viruses, these viral fragments are often extracted from the insect vectors that ferry the viruses from plant to plant.

Mysteries abound in the viral world. Scientists still aren't quite sure where they came from. The illustration describes three leading theories. According to the virus-first hypothesis, RNA molecules capable of enzymatic activity and self-replication preceded cellular forms at the dawn of life. According to the reduction hypothesis, viruses came from small primordial cells that lost their cellular elements in the course of evolution, while retaining their genetic material and the machinery required for replication. According to the escape hypothesis, viruses arose from cellular RNA or/and DNA fragments such as plasmids and transpozons. During cell fission, a smaller cell-like entity may have formed, engulfing a self-replicating RNA fragment and a coat-encoding RNA segment, forming a virus. Graphic by Shireen Dooling 

New methods uncover a welter of new viruses

Metaviromic sequencing is a particularly powerful technique for investigating viral communities. Unlike cellular life, which has a single, common origin, viruses are polyphyletic, meaning that they are the result of multiple origins. No single gene has been identified that is shared by all viruses. While common protein motifs have been observed in viral capsids, these are likely the result of convergent evolution or horizontal gene transfer, rather than inherited elements.

The strategy of metaviromics is particularly useful for teasing out mutualistic relationships between plants, vectors and viruses and their changing relationships over time. As so much research since the inception of virology has been focused on viruses as disease-causing agents in humans and plants, the nature and degree of mutualistic interactions between viruses, vectors and hosts is most likely underrepresented.

The authors speculate that viruses may play an important role in maintaining biodiversity and helping plants adapt to their environment by limiting the growth of genetically homogeneous plants, including crops. New studies of viral ecology seek to understand the extent and importance of both pathogenic and mutualistic interactions. An all-important link in the chain of infection is the behavior of particular insect vectors and their modes of viral transmission, though numerous other factors come into play, including nutrients, water resources, heat and cold stress and adverse soil conditions.

Viral intermediaries

Vectors play an outsized role in the world of plant viruses. Unlike animal viruses, plant viruses are not usually transmitted through direct contact between infected and uninfected individuals. Instead, plant viruses disseminate through vectors (especially insects), as well as through pollen and seeds.

It is believed that the mode of viral transmission plays a role in the virus’s effect on its host. If the virus is transmitted via seeds or pollen, the virus should limit its harmful effect on the reproductive success of the host plant, perhaps even conveying an adaptive advantage over uninfected plants.

The viral passage from parent to daughter plant is known as vertical transmission. By contrast, horizontal viral transmission occurs when insect vectors transit the virus from plant to plant. Such vector-borne assaults can be more merciless to the infected plant and only need ensure their continued spread to a suitable number of healthy plants for the virus to be successful.

Many kinds of vectors can transmit plant viruses, including arachnids, fungi, nematodes and some protists, though more than 70% of known plant viruses are transmitted by insects, most from the biological order Hemiptera, which includes cicadas, aphids, planthoppers, leafhoppers and shield bugs.

Insects of this kind can make use of mouthparts constructed for piercing and extracting sap or plant cell material. Insect transmission of plant viruses can occur through excretion of virus particles in saliva following feeding on an infected plant. Alternately, the plant virus can become permanently incorporated into the insect’s salivary glands, allowing the vector to transmit the virus to new plants throughout the insect’s lifetime.

Intriguingly, a number of insect-transmitted plant viruses may have evolved mechanisms to influence vector behavior, making infected plants more attractive to sap-feeding insects or ensuring that infected plants produce chemicals that promote insect behaviors that help facilitate transmission.

In addition to their complex and varied chains of infection, some plant viruses have another unique property. Such viruses transmit their genomes in multiple packets, each containing only part of the virus’s complete genetic code, encapsulated in a separate virus particle. This peculiar strategy, which requires the co-transmission of several viral particles to a new host in order to ensure the integrity of the viral genome, is a feature believed to be unique to plant viruses. The nature and evolution of these so-called multipartite viruses remains a biological puzzle. 

Plant viruses display considerable ingenuity in their strategies, which are highly dependent on their given environment. Some are generalists, invading multiple species, while other viruses are specialists that favor a narrow range of plant hosts. This selectivity may develop with time, through a process known as adaptive radiation. This typically occurs when a virus faces a heterogeneous habitat and becomes adaptively specialized to exploit particular ecological resources while becoming maladapted to exploit others. Such specialization acts to limit competition between different viral lineages or species. Alternatively, generalist viruses infect multiple plant hosts but must compete for these resources with other viruses. This situation tends to result in a viral population of low diversity dominated by the most acutely adapted viral genotypes.

The arrival of viruses

While researchers agree that viruses lack a single common ancestor, a detailed picture of how (and when) they emerged in the web of life remains deeply contested. Three common hypotheses compete for dominance as an explanatory framework, though they are not mutually exclusive. Perhaps viruses evolved from free-living cells, as the devolution or regressive hypothesis states. They could also have originated from RNA and DNA molecules that somehow escaped from living cells. Alternatively, viruses may have once existed as self-replicating entities that evolved alongside cells, eventually losing their independent status.

Ongoing metaviromic research of viral diversity is helping to uncover foundational relationships among viruses and pinpoint common origins among many plant, fungal and arthropod viruses. Of particular concern for the future are the ways in which human-caused disruptions to ecosystems across the planet, which are occurring at rates unprecedented in Earth’s history, are reforming virus, vector and host relationships.

The effects of these disruptions may be to foster emergent viruses with heightened abilities to cause disease in their hosts.  As ecological communities become more tightly interwoven through changes in human land use, existing interaction networks that have acted over evolutionary time to stabilize host relations with native vectors and viruses can suddenly shift. Any lethal entity entering this kind of disrupted ecosystem is much likelier to rapidly spread through the population and aggressively sweep through different organisms. The future health and sustainability of both human and plant populations will benefit from an improved understanding of the many subtle interrelationships governing the most ubiquitous viruses — those colonizing plants.

Richard Harth

Science writer, Biodesign Institute at ASU


ASU Law alumna recognized as one of the most influential women in Arizona business

Tonya MacBeth talks about her professional detour to an acclaimed legal career

July 17, 2019

Most lawyers spend years preparing for law school. Tonya MacBeth, a 2005 graduate of the Sandra Day O’Connor College of Law at Arizona State University, is not most lawyers.

After studying psychology, sociology and Spanish as an undergrad, she spent a decade working in the mental health field when her career hit a sudden roadblock. The advocacy work that she had been contracted to do with the state of Arizona was under a class-action lawsuit, and the litigants in the case were requiring a lawyer to be in charge of the state agency. photo of Tonya MacBeth Tonya MacBeth is a 2005 graduate of ASU Law and has been recently named a Most Influential Woman in Arizona Business. Download Full Image

The stakeholders apologetically told MacBeth she wouldn’t be eligible to lead the agency, despite her years of dedicated service.

“Being the Type A person that I am, I couldn’t imagine spending the rest of my career being second fiddle,” she said. “So I thought, I better go to law school.”

The last Law School Admission Test that could be taken that year was a mere 30 days away. She had never before considered law school, and she had been out of college for 10 years. But she was undeterred.

“I sat down with the LSAT study books and decided to really dive in to the questions and go for it,” she said, reasoning that she had a fighting chance to pass it because the test is more about problem-solving and vocabulary than legal issues. “So I studied for the LSAT, applied to ASU, just barely got in under the application deadline, went to law school, and never looked back.”

It was a major turning point in her career, and when she graduated from law school, she had different goals in mind. She credits her experience at ASU Law — the clinical work and the engaging professors — with broadening her horizons. And she was concerned that if she went right back to her previous government work, she would never have any other options.

“Coming out of law school, and having had the mental health and government experiences, I thought it was very important to have the experiences being a litigator,” she said. “Because a litigator versus an administrator, it's very different work.”

Knowing very few lawyers upon graduation, she was determined to build a network. So she rolled up her sleeves and began with an old-fashioned letter-writing campaign.

“That was back when we actually wrote letters,” she recalled with a laugh. “I wrote letters to prominent attorneys in the Valley that I had known of, through news reports and magazine articles — the movers and shakers in town — and asked them to have coffee with me. And when I met them, at the end of the coffee, I would say, ‘If you know of anybody who’s hiring, here’s my resume, and please feel free to forward it on.’”

One of those attorneys she met with was Chip Harris, who was one of the top civil, personal injury and medical malpractice attorneys in the Valley. And when she handed him her resume and told him to pass it along to anybody who might be hiring, he just laughed.

MacBeth recalled, “He said, ‘Well, what’s wrong with me? Why can’t I hire you?’”

And that’s how her legal career began, at the Harris, Powers & Cunningham law firm. A few years later, while working at her next firm, after a particularly interesting case came to a close, she called the opposing counsel, Ian Neale, and asked if he would meet for lunch. Much like her meeting with Harris, that lunch led to an employment offer to join the Burch & Cracchiolo firm. She joined in 2008 and has been with the firm ever since.

“It just goes to show that reaching out and making those personal connections really does still work,” she said. “We can talk about networking on LinkedIn, or email or whatever. But having those face-to-face meetings is where things really happen.”

She initially worked in civil litigation for Burch & Cracchiolo, focusing on construction defect and defense work, but when an opportunity arose to move into family law, she jumped at the opportunity to get closer to her career roots.

“I love it — it’s a perfect practice for me,” she said. “I'm a rational, reasonable person who has enough mental health background to know to handle it when people are in crisis and keep the focus on what needs to get done, to accomplish the larger financial and long-term parental goals without getting into the weeds on the interpersonal conflicts.”

It’s difficult work but highly gratifying, because of the personal stakes her clients have in the cases.

“I really enjoy this particular practice area, because clients really care about the outcomes,” she said. “Having done insurance defense work, it's a different level of intensity and different level of interest in the outcome. For insurance companies, it's a dollars and cents cost-benefit analysis. But in family law, these are people's lives. So if you're going to stay up until 3 o'clock in the morning, it might as well be thinking about somebody's future as opposed to concrete thickness.”

MacBeth is now a shareholder in the firm and remains active in the community. She serves on the board for the Arizona Center for Law in the Public Interest, and chairs the advisory board for the CHEEERS Recovery Center, a peer-run recovery program focused on individuals and families affected by behavioral health conditions, and is active in state and county politics, having run twice for the Arizona Legislature. Az Business magazine recently named her one of the 50 Most Influential Women in Arizona Business, an annual list that recognizes the state’s female leaders for their impact on their organizations, the region’s business climate and the local community.

“It was a real honor to know that my involvement in the community and my law practice as a whole does have an influence on the direction of the Valley,” she said, recalling her surprise when she received the 50 Most Influential Women recognition. “And it’s not just me, but it’s all the people I work with through all my endeavors that I bring together that made this happen.”

It’s an honor she said she never could have imagined years ago, when she was a mental health advocate suddenly cramming for the LSAT and hoping to get into ASU Law.

“I was very fortunate that ASU allowed me to attend, and I can’t imagine what would have happened if they had said no,” MacBeth said.

And she is thankful to Burch and Cracchiolo for unwavering support of her community service.

“The firm has been very supportive of that community engagement, and I really feel that that helps me be a better lawyer, because I'm out in the world, I'm not just in my books,” she said. “And I really love Arizona and I love the Valley, and I want to make it as strong a place as possible. I love being out there, engaging in different endeavors. Whether it's politics or community service, mental health services, it all comes together to make the web that supports Phoenix stronger.”

Nicole Almond Anderson

Director of Communications, Sandra Day O'Connor College of Law