Globe-trotting virus threatens tomato crops

ASU molecular virologist and colleagues track the metamorphosis and spread of TYLCV

January 12, 2017

Tomatoes, prized for their delicious taste and high nutritional content, are one of the most important crops grown around the world. In recent years, however, tomatoes have come under assault from a persistent and aggressively spreading pathogen.

Known as tomato yellow leaf curl virus (TYLCV), the microbe has undergone rapid expansion from its humble origins in the Jordan Valley in the Middle East. Today, TYLCV devastates cultivated plants in both tropical and subtropical regions and has proven particularly difficult to control. It can often cause 100 percent destruction of tomato crops. Biodesign researcher Arvind Varsani Arvind Varsani, a researcher in the Biodesign Center for Fundamental and Applied Microbiomics, has been tracking the global spread of the disease-causing tomato yellow leaf curl virus. Download Full Image

Arvind Varsani, molecular virologist at Arizona State University’s Biodesign Center for Fundamental and Applied Microbiomics, has been tracking the global spread of this disease-causing virus, which is usually transmitted by an insect vector, Bemisia tabaci, better known as the silverleaf whitefly.

Varsani’s global search for novel and persistent viruses has taken him to remote regions of the world, where he has catalogued the presence of these tiny entities in everything from desert sands to Antarctic permafrost — a viral landscape of almost unfathomable richness, of which less than 1 percent has so far been explored. (Viruses, unlike bacteria and other members of the microbial world, do not have a universal gene, rendering them difficult to classify.)

Safeguarding the global food supply from disease-causing pathogens is a growing challenge. Habitat loss around the world is improving conditions for viral transmission and evolution as varied species come in closer contact. Keeping pathogens in check will require better techniques for identifying these viruses and managing global epidemics.  

In a study recently published in the journal Virology, Varsani and his colleagues provide the most detailed accounting to date of the metamorphosis and spread of TYLCV. Their results highlight the challenges involved in controlling the virus, given the rapid emergence of variants able to survive targeted pesticides and outwit tomato varieties bred for resistance — the two mainline approaches used to combat the disease.

“It is impressive to see how quickly TYLCV has spread across the world from its most probable ‘tropical hub’ in the Middle East and eastern Mediterranean region,” said Varsani, who is also an associate professor in the School of Life Sciences. “Furthermore, despite the strong quarantine regulations in place in various countries such as Australia, there have been multiple introductions of TYLCV. In general, geminiviruses are known to have high mutation rates and are highly recombinogenic, allowing them to explore sequence space rapidly.”

Tomato yellow leaf curl virus graphic

This graph shows the timing of historic movements of the tomato yellow leaf curl virus between the 12 regions analyzed in the study. The color gradients in each line show the potential movements from the ancestral variants of the virus (on the left of the line) to the migratory destination (represented by the color on the right of the line).

As the study notes, TYLCV is established in many tomato-growing regions of the world and continues to spread to new regions around the Indian and Pacific oceans including Australia, New Caledonia and Mauritius. The research provides a time-sensitive analysis of all publicly available, full genome sequences of TYLCV, together with 70 new genome sequences from Australia, Iran and Mauritius.

Viral mileage markers

Viruses provide excellent tools for monitoring evolutionary change over time and across geographic expanses, due to their rapid mutation rates and fast generation times. The current study makes use of this fact, exploiting a technique known as phylogeographic analysis to understand the origins and distributions of different viral strains.

Phylogeography produces evolutionary trees that combine genetic data with spatial information. Drawing on the increasing availability of genetic and geospatial data, phylogeography has also been used to track the global dissemination of many important disease-causing pathogens in humans, including viruses responsible for dengue fever, rabies, influenza and AIDS. Subtle alterations in viral genetic sequence can act like identifying fingerprints that offer information about where the particular strain originated and how rapidly it has evolved.

Mathematical models integrating spatial data on pathogen evolution with information on vectors, plant movements and environmental variability can provide researchers with vital clues helpful in managing disease epidemics in plants and animals including humans, while also advancing fundamental knowledge of evolutionary and ecological processes.

A tomato’s worst adversary

TYLCV is a circular, single-stranded DNA virus belonging to the family Geminiviridae. It is the most destructive member of a related group of pathogens causing tomato yellow leaf curl disease (TYLCD). While it is typically spread by an insect vector, recent research has shown that unlike other viruses of the same genus (Begomovirus), TYLCV is also seed transmissible. This fact, combined with the rapid development of resistant variants, has presumably led to TYLCV’s brisk migration and tenacious persistence.

The study results indicate that the first viruses belonging to the TYLCV strain likely arose in the Middle East between the 1930s and 1950s. They were not identified until the early 1960s and probably began their global conquest in the 1980s, when two strains, TYLCV-Mld (mild) and TYLCV-IL (Israel) spread outward from the Jordan Valley.

An outbreak in the eastern Mediterranean may have provided the virus with its first opportunity to spread to the rest of the world, eventually arriving in most tropical and subtropical regions and earning the distinction as one of the most devastating plant pathogens.

Map showing the spread of the tomato yellow leaf curl virus

The map shows the global migration patterns of the tomato yellow leaf curl virus. Eighteen epidemiological links between 12 geographic regions identified in the study are displayed. The thickness of the lines represents the number of independent movements between locations. Dashed and solid lines indicate the "Bayes factor" — a measure of probability based on the gathered data.

Although seven major strains of TYLCV have been identified, only TYLCV-Mld and TYLCV-IL have ever been identified outside of Iran, the epicenter of TYLCV activity. (The diversity of TYLCV in Iran may be due in part to the climate, which has warmed and dried in recent years, creating conditions highly conducive to the whitefly carriers of the virus, though these fast-evolving strains are not considered a global threat at present due to epidemiological isolation of the region.)

As the study notes, the Mediterranean basin is the likely staging area for global movement of TYLCV. TYLCV-IL and TYLCV-Mld have the broadest geographical ranges of any TYLCV strains, and their dominance stretches in the Old World from Japan in the east to Spain in the west and the Indian Ocean island of Reunion and Australia in the south.

Presently, the virus is aggressively spreading into North and South America. The problem is partly due to ubiquitous international trafficking of crop varieties, though among geminiviruses, the geographical range — particularly of TYLCV-IL — is uncommonly broad. This highly invasive strain appears to have been introduced to the Americas, once from Australia and at least thrice from East Asia.

Infection sequence

While some notorious viruses (influenza, Ebola, HIV) may be spread through aerosol transmission or bodily fluids, many viral pathogens infecting plants and animals require a vector to pierce protective flesh or abrade plant tissue in order to introduce the viral particles or virions into cells. TYLCV is one such virus, requiring an insect intermediary to complete the infection process.

The disease is transmitted by the silverleaf whitefly, which acquires the virus after feeding on an infected plant for 15-30 minutes. After a latent period within the insect of 18-24 hours, the virus will be transmissible and a single whitefly may infect multiple plants. Large swarms of whiteflies can move between crops, causing rapid and far-reaching devastation. Some evidence suggests whiteflies may be able to pass on the virus to offspring, though this remains speculative.

Symptoms of viral infection by TYLCV include stunted plants with affected leaves showing curling, discoloration and deformation. The younger the plants are at the time of infection, the more severe is the reduction in yield. 

Over long distances, the virus is primarily spread through the movement of infected plants. Since symptoms can take up to three weeks to develop, infected specimens often go unnoticed. Whitefly carriers of the virus also often hitchhike with plants, providing another means of long-range viral migration.

Evading resistance

Viruses like TYLCV can mutate rapidly. When two or more variants of the virus enter plant cells, they may swap portions of genomes, known as recombination. Through recombination, viruses aggressively shuffle the genetic deck, in the process producing novel strains capable of outwitting hybridized plant resistance.

Using phylogeography, Varsani and his colleagues describe in detail the complex variables affecting past and present-day global migrations of TYLCV. While epidemics in Australia and China are the likely result of multiple independent viral introductions from the East Asian region around Japan and Korea, the New Caledonian epidemic is derived from a variant from the western Mediterranean region and the Mauritian epidemic by a variant from the neighboring island of Reunion. Research suggests that intercontinental scale movements of TYLCV to East Asia have temporarily ceased, while long-distance movements to the Americas and Australia are likely ongoing.

Varsani notes that a better understanding of transmission dynamics and global pathways of migration will be required in order to develop better methods of control. Conditions for viral transmission are rapidly changing as humans come in greater contact with each other and with habitats harboring pathogens and global travel speeds up viral transmission and evolution.  

At the same time, ancient viruses may be poised to re-emerge as environmental conditions change; for example, the exposure of unknown viruses locked in permafrost and released due to global climate change — another area of active research by Varsani and his colleagues.  

Richard Harth

Science writer, Biodesign Institute at ASU


ASU and partners to bring clean water to Middle East communities

USAID awards nearly $2 million for research and development of holistic solutions; cross-disciplinary project is tackling legal, cultural and technical angles

January 12, 2017

An Arizona State University-led global consortium of technology and in-country partners will implement a two-year, $1.95 million USAID project to develop and test affordable, portable clean water solutions in the Middle East. 

Communities across the Middle East are facing severe water shortages. Some communities rely on limited and variable water supplies without the infrastructure to adequately treat and transport the water. Energy sources needed to purify water can be inaccessible, expensive, or unreliable. Local utility experts discuss the water quality details with ASU professor Rhett Larson for a well under consideration in Qubbe, Lebanon. Anthonio Moawad (center), project manager at the René Moawad Foundation, and ASU professor Rhett Larson (right) discuss the water-quality details of a well under consideration in Qubbe, Lebanon, with a local utility expert (left). This site is being considered as the first for implementation and would provide purified water to people in Bab El Tebbeneh, one of the poorest communities in Lebanon. Photo by Ashley St. Thomas/ASU Walton Sustainability Solutions Initiatives Download Full Image

Population needs and challenges associated with the growing influx of refugees from neighboring countries, such as Syria, have exacerbated the problem, frequently making water a source of dispute between communities. In some instances, the relationship between local customs and constitutional governance, including different interpretations of the laws that govern water rights and water pricing, affect how water resources are developed and managed.

The USAID project, "A Holistic Water Solution for Underserved and Refugee Host Communities in Lebanon and Jordan," will be implemented in 18 communities throughout Jordan and Lebanon, benefitting more than 36,000 people. The scalable model will be established in accordance with community-specific legal and cultural frameworks.

An interdisciplinary team from ASU, ranked by US News as the No. 1 school in the nation for innovation, is spearheading this project by providing expertise in sustainability, law and engineering. The team comprises Richard Rushforth, a project manager for the Walton Sustainability Solutions Initiatives; Rhett Larson, a professor with the Sandra Day O’Connor College of Law and an expert in Middle East water policy; and Nathan Johnson, an assistant professor at the ASU Polytechnic School, one of the six Ira A. Fulton Schools of Engineering. They are joined in the consortium by public and private partners from across the globe focused on water security and development: H2O for Humanity (Illinois), GreenCo Water (Australia), Mercy Corps (a global development organization), the René Moawad Foundation (Lebanon), and Zero Mass Water (Arizona).

“Having strong implementation partners is integral to the success of this project,” Rushforth said. “USAID demonstrated solutions-oriented global leadership with its new co-creation project development model, which allowed us to build relationships with world-class partners, providing greater, more immediate impact to communities and people in need throughout Lebanon and Jordan.”

The consortium took shape through preliminary meetings led by ASU. Larson was familiar with H2O for Humanity’s success with groundwater-treatment kiosks in India as well as the René Moawad Foundation’s renowned reputation serving rural populations in Lebanon. Rushforth, along with Joshua Fine, a project development associate at the René Moawad Foundation, participated in the co-creation workshop where Zero Mass Water, led by ASU’s Cody Friesen, and GreenCo Water were brought into the fold. Mercy Corps joined the consortium as its implementing partner in Jordan in February 2016.

“Water is inherently interdisciplinary. You cannot develop water without considering environmental, technical, economic, cultural and legal issues,” Larson said. “Our team is made up of experts in all areas of water policy and management, which makes this project especially exciting. We have a chance to truly help thousands of people in need.”

The consortium has developed a holistic water system that operates at the household and community levels by making use of nontraditional water resources in order to avoid further depleting the region’s scarce groundwater supply. Each system includes H2O for Humanity’s water purification kiosk (AquaSafi) to purify water through reverse osmosis that eliminates salts and contaminants. Two systems will be equipped with an enhanced power supply system.

“In order to provide clean water, we must first ensure there is reliable power,” said Johnson, whose primary goal is to design, integrate and deliver an optimized power system. “Since the kiosks are currently connected to the grid — which is unreliable for up to several hours a day — we need to provide sustainable, reliable power to run the water treatment system.”

Local utility experts discuss the water quality details with ASU professor Rhett Larson for a well under consideration in Qubbe, Lebanon.

Hasan Daouk of Zero Mass Water (left) and ASU professor Rhett Larson discuss placement of H2O for Humanity’s AquaSafi-2000 water purification system in the existing kiosk at an out-of-use well in Qubbe, Lebanon. Photo by Ashley St. Thomas/ASU Walton Sustainability Solutions Initiatives

At the household level, Zero Mass Water’s technology (SOURCE) will allow families in Lebanon and Jordan the opportunity to own their own water source for the first time. These household solar panels convert atmospheric water vapor into clean drinking water, even in the semi-arid and arid climates of the Middle East. Combining these two technologies with GreenCo Water’s Pak-Flat Tank — a 1,000-liter tank that ships flat-packed in a box and can be assembled in less than 10 minutes — will increase available potable water in the selected communities by 20 percent.

The René Moawad Foundation and Mercy Corps — the project’s implementing partners in Lebanon and Jordan, respectively — will conduct trainings for women (in collaboration with women’s cooperatives in the selected communities) to manage the water kiosks and generate income. The implementing partners will also conduct awareness-raising campaigns on water-demand management. The holistic water systems will be operational in Lebanon and Jordan in the spring of 2017.

Jason Franz

Senior manager, Marketing and Communications, Walton Sustainability Solutions Initiatives