In California’s San Joaquin valley, it is citrus season. An open-air warehouse on the out-skirts of Dennis Johnston’s 600-hectare cit-rus grove brims with huge crates of oranges,

mandarins and grapefruits. This year, his farm will ship around US$8-million to $10-million worth of citrus around the United States and the Pacific Rim.

Cruising through the labyrinthine dirt roads that criss-cross his farm, Johnston surveys the winter crop, passing tree after tree, each a mop of dark green dotted with baseball-size fruits.

The trees are productive and the fruit healthy, but in the back of Johnston’s mind is the pos-sibility that trees could fall sick from insect-spread infections. Tristeza virus, for instance, fells a tree every few years, he says. Johnston is vigilant. He serves on his county’s pest-control board and educates other growers about plant diseases that range from minor nuisances to epidemics that could ruin the San Joaquin val-ley’s billion-dollar citrus indus-try. “We have a hard time getting growers to understand the sever-ity of these bacterial and viral infections,” says the easy-going third-generation grower.

Green alertMention huanglongbing, and Johnston cringes. “We were being warned by the scientists and the people in the know that this is a serious, serious thing and we’ve got to, at all costs, keep it out of the valley and keep it out of Califor-nia,” he says.

Named for the colour of the infected leaves, huanglongbing is Chinese for yellow dragon disease. It is a bacterial infection that spreads from tree to tree via citrus psyllids, drain-ing nutrients from the plant and resulting in diminutive green fruits, thinning branches and eventually death of the tree. It has devastated the citrus industry in many Asian countries, killed hundreds of thousands of trees in Brazil, and

swept through 26 Florida counties since it first arrived on US soil in 2005. It is considered the most dangerous citrus pathogen in the world.

The US government agrees. The bacterium that causes the disease, ‘Candidatus Liberib-acter’, comes under the same regulations that restrict research on Ebola, anthrax and other microbes that have been deemed potential agents of terror. An attack on the food supply with a plant pathogen such as ‘Ca. Liberibacter’, some say, could have disastrous effects on the nation’s economy. Researchers who study these ‘select agents’ must submit to background checks by the Federal Bureau of Investigation (FBI), install extra security outside their labs, and file mounds of paperwork.

These measures are necessary, the govern-ment says, to keep the pathogens from falling into the wrong hands. A terrorist-spread epi-demic of huanglongbing, for instance, could kill millions of trees and rattle consumer con-

fidence, says Jacqueline Fletcher, director of the National Institute for Microbial Forensics and Food and Agricultural Biosecurity in Stillwater, Oklahoma.

Other scientists, though, say that treating ‘Ca. Liberibacter’ and other emerging plant patho-

gens as potential agents of terror leaves grow-ers such as Johnston worse off. Slapping the select-agent status on plant pathogens inevi-tably means that fewer researchers can study the organisms, slowing the development of countermeasures. Compliance with the strict regulations is costly and time-consuming, researchers say. And officials in Florida con-tend that the bacterium’s select-agent status sapped their response to the 2005 outbreak of huanglongbing, which continues to rage. Diagnostic tests have been slow to develop and researchers still haven’t figured out how to grow the bacterium in the lab.

“There’s no question that select-agent type

regulations are necessary for Ebola virus and 1918 influenza,” says Caitilyn Allen, a micro-biologist at the University of Wisconsin–Madi-son. “The question that needs to be considered seriously is whether these plant pathogens pose a similar risk.” Indeed, the US government is now deliberating changes to the select-agent list to reflect the growing prominence of huan-glongbing in Florida.

The war on agroterrorIn 1996, the US government created its first list of select agents, after Larry Wayne Harris, a microbiologist and white supremacist, tried to purchase vials of the bacterium that causes bubonic plague. The initial list included patho-gens in humans and animals, but not plants.

But biosecurity soon became an important issue for plant pathologists too. In 1999, the American Phytopathological Society in St Paul, Minnesota, hosted a well-attended symposium on the potential for plant pathogens to be used as weapons. That same year, the organization issued a statement recommending better sur-veillance of plant-disease outbreaks, eyeing the possibility of agroterror.

Those flirtations with biosecurity turned serious after letters laced with anthrax started appearing in the US mail system shortly after the ter-rosist attacks of 11 Septem-ber 2001. Fletcher was then president-elect of the Ameri-can Phytopathological Society. In February 2002, she and several other scientists briefed Congress on the potential for plant pathogens to be used by terrorists. “While there is no evidence that agriculture might be a current target of terror-ism, September 11 has made us all more aware of the need to be prepared for any possibility,”

Huanglongbing, a disease that could devastate the US citrus industry, pits national security against plant pathologists looking to battle natural

outbreaks, Ewen Callaway reports.

The greenmenace

“Huanglongbing is a disease that can wipe out citrus as we know it.” — Larry Bezark

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Fletcher said at the time. Congress and President

Bush listened. On 12 June that year, Bush signed the Agricultural Bioterrorism Protection Act, ordering the US Department of Agriculture (USDA) to include plant pathogens on the select-agent list. Two months later, the agency began enforcing the law, listing nine plant pathogens, including two species of ‘Ca. Liberibacter’ (see ‘The select few’).

To ensure flexibility, the USDA included only exotic pathogens — those usually found outside the United States — as select agents and mandated that they be removed from the list once they took hold in the country. The law would be updated every two years to accomo-date such changes, although not until extensive consultation has been done.

Some researchers view this elevation of status as a boon. “Having the select-agent list helps us to prioritize,” says Fletcher. “It also targets special funds for working on those things if they should come in.” Indeed, the USDA’s biodefence budget bloomed from $200 million in 2003, the first year that numbers were made avail-able, to $340 million in the 2008 budget, according to the Center for Biosecurity at the University of Pittsburgh Medical Center in Baltimore, Maryland.

Heightened awareness of plant pathogens also spurred the USDA to establish a national network of laboratories to diagnose plant diseases. Before 9/11, every state ran its own plant-pathology lab, each of which had dif-ferent procedures for testing diseased plants. But funding was scarce and “all these labs were languishing”, Fletcher says. Although agroter-rorism was the motivation behind the long-

overdue network, improved diagnostics and communication between state labs

will speed the response to any out-break, she says.

On 23 August 2005, plant pathol-ogists had their worst fears real-ized: huanglong-bing was found in the pomelo trees of two homeowners

near Miami. Ten days later, the USDA confirmed the diagnosis. In the months that followed, officials found the disease in thousands of trees in most of Florida’s citrus-growing counties.

Where it came from no one knows, but historical records suggest that the disease originated in the Guangdong province in southern China or in central India in the late 1800s. It quickly sped through Asia, where one species, ‘Ca. L. asiaticus’, is now endemic from Japan to Pakistan. A second species, ‘Ca. L. africanus’ is found throughout eastern, central and southern Africa, and a third species, ‘Ca. L. americanus’ has been discovered in Brazil.

Yellow dragonCitrus trees infected with huanglongbing show few symptoms for several years. Eventually,

their leaves develop character-istic yellow splotches, and trees produce puny, discoloured fruit. Production drops rapidly, until the trees eventually die. Worse, infected trees churn out bacteria for the psyllid to cart elsewhere.

Given the havoc the disease has wreaked around the world, there is good reason to worry that huanglongbing will spread throughout the United States, says Phil Berger, acting director of the USDA’s Center for Plant Health Science and Technology in Raleigh, North Carolina. A survey in the late 1990s estimated that 53 million trees in Asia were infected with huanglongbing, and 10 million in Africa. A systematic survey of the Reunion Islands in the 1980s found that huanglongbing had killed 65% of their citrus trees within seven years of planting. And in parts of northern Thailand, the bacterium kills at least one-tenth of tangerine trees every year. In the state of São Paulo in Brazil, an estimated 800,000 trees have been lost since an outbreak hit in 2004.

As the citrus pysllid moves west from Florida — it has turned up in Texas and Mexico — offi-cials and growers are preparing for the worst. “The threat is enormous,” says Larry Bezark, of the California Department of Food and Agri-culture in Sacramento. Bezark spearheads the state’s response to huanglongbing — scouring farms, nurseries and even ports for psyllids and infected plants. “This is a disease that can wipe out citrus as we know it,” he says.

The psyllid bug (left) carries the

bacterium that causes huanglongbing in citrus.

“Few, if any, plant pathogens should be considered bioterror agents.” — Tim Gottwald

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But while California prepares for an out-break, researchers and officials in Florida feel handcuffed by the pathogen’s continued status as a select agent, even though it is now wide-spread in Florida. “We had our hands tied,” says Wayne Dixon, chief of plant pathology at the Florida Department of Agriculture and Com-merce in Gainesville. Whenever a sample from a tree turns up positive, the select-agent law mandates that the lab notify the USDA and destroy the sample within a week. This com-plicates efforts to perform additional diagnos-tics, says Dixon, who supports listing some exotic plant pathogens as select agents but not ‘Ca. Liberibacter asiaticus’.

To comply with the select-agent listing, researchers must register with the federal gov-ernment, install added security to their labs such as video mon-itors and fingerprint-accessed doors, and submit to background checks. For-eign researchers have an especially hard time getting approved to work on select agents. The penalties for violating the law are harsh — up to $250,000 and five years in jail.

Species swapIn August 2007, the USDA proposed updating the select-agent list to remove the asiaticus spe-cies found in Florida, while adding the Brazil-

ian americanus species to the list. It is now reviewing the comments

it received on its proposals, which are overwhelmingly

in favour of lifting the select-agent status of

the asiaticus spe-cies — and

hopes to issue a final rule later this year, says Michael Firko, a USDA official who is leading the agency’s efforts.

While the proposal to remove the asiaticus strain from the select-agent list seems to be headed for approval, several other plant patho-gens may be added, including diseases of soya, rye, woody trees and shrubs, and rice.

The proposed addition of a strain of the rice pathogen Xanthomonas oryzae has left some microbiologists scratching their heads. The cause of leaf streak in rice, X. oryzae has done significant damage to crops in Asia and Africa.

Yet the pathogen is unlikely to take hold in the United States because of different farming practices and a hostile climate, says Leach, who studies the bacterium.

The added cost of complying with the select agent rule may force some researchers to aban-

don their work on X. oryzyae. “I stay up late at night worrying about this stuff,” says Pam Ron-ald, a geneticist at the University of California in Davis who studies the rice pathogen

Firko contends that the select-agent status of ‘Ca. Liberibacter asiaticus’ hasn’t hampered research. “We have not refused registration to anybody for this agent, and I don’t think we have refused any experiment that people want to do.”

Classifying ‘Ca. L. asiaticus’ as a potential agent of bioterror is paradoxical, says Eric Triplett, a microbiologist at the University of Florida in Gainesville. “It doesn’t make sense to have such enormous restrictions on labora-tories and confine it to strict BSL-3 conditions when it’s already outside our window.” To study the disease, Triplett and his lab members must

travel to a facility 225 kilometres away that has been approved specifically for work on select agents. The microbiologist would like a lab of his own to work on huanglongbing, but the government has yet to approve it.

“Few, if any, plant pathogens should be con-sidered bioterror agents,” says Tim Gottwald, a plant pathologist at the research wing of the USDA in Fort Pierce, Florida, who stud-ies huanglongbing. Gottwald estimates that he spent $50,000 upgrading his lab to comply with the select-agent rules. More troubling, he says, are delays in getting scientists approved to work on the disease. “I have 12 to 14 people somewhere in the FBI black hole,” he says.

The pathogen’s select-agent status may also scare away promising young scientists because the restrictions slow down the progress of research, says Triplett. “It’s very hard to persuade a post-doc or grad student to work on a project when it’s going to hamper [his] career,” he says.

More than 3,000 kilometres away, Johnston has his own worries as he scans his grove at the end of a long day. He stops at a navel tree and plucks a shoulder-high fruit, then slices the orange open with a couple of quick motions of a pocket knife. Its juice squirts out and the tangy perfume fills the air for a second. Huan-glongbing would reduce the sweet fruit to a withered, bitter gall.

Meanwhile, Johnston says that he hasn’t even heard of the select-agent rule. “I am much more concerned that the US government, through inaction, will allow this stuff to move from Florida to Texas to California.” When asked about agroterror, he laughs and points out that those wishing to do harm could pick a better weapon than huanglongbing. “Are they going to try to kill orange trees rather than people? I doubt it.” ■

Ewen Callaway is a science journalist in Washington DC.

See Editorial, page 127.

THE SELECT FEW

Microbe Disease Select agent status

‘Candidatus Liberibacter africanus’ Huanglongbing Current

‘Ca. L. asiaticus’ Huanglongbing Current

Peronosclerospora philippinesis Philippine downy mildew of corn Current

Ralstonia solanacearum, race 3, biovar. 2 Brown rot of potato Current

Sclerophthora rayssiae var. zeae Brown stripe downy mildew of corn Current

Synchytrium endobioticum Potato wart disease Current

Xanthomonas oryzae pathovar. oryzicola Rice leaf streak Current

Xylella fastidiosa (citrus variegated chlorosis strain)

Citrus variegated chlorosis Current

Phakospora pachyrhizi Asian soya bean rust Removed 2005

Plum Pox potyvirus Plum pox Removed 2005

‘Ca. L. americanus’ Huanglongbing Proposed 2007

X. oryzae pathovar. oryzae Rice leaf streak Proposed 2007

Phoma glycinicola Ref leaf blotch of soya bean Proposed 2007

Phytophthora kernoviae Related to sudden oak death Proposed 2007

Rathayibacter toxicus Gumming disease in ryegrass Proposed 2007

“It doesn’t make sense to have such enormous restrictions when it’s already outside our window.” — Eric Triplett

Are the complex rules and regulations governing select agents stymying work to study and monitor the spread of huanglongbing (HLB)?

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Leak leaves Antarctic observatory blindedA robotic observatory atop a plateau in eastern Antarctica has shut down after an exhaust leak caused its generator module to overheat. A Chinese expedition installed the PLATeau Observatory (PLATO) in January at Dome A, the highest point in eastern Antarctica at 4,100 metres altitude (see Nature 451, 752; 2008). The observatory had operated continuously for 204 days before the leak. It is hoped that solar power will revive some of PLATO’s instruments by the end of August, as spring nears.

PLATO has four 14.5-centimetre telescopes and weather instruments to test conditions at the site, which is one of the coldest and driest places on Earth. The Polar Research Institute of China has plans to return to the site next year to add three 50-centimetre telescopes.

US ocean agency upgrades its research fleetThe US National Oceanic and Atmospheric Administration (NOAA) has retired the last of its wooden-hulled ships on the same day it commissioned a modern research vessel.

On 13 August, the John N. Cobb was retired in Seattle, Washington, after 58 years of service. The ship conducted fishery studies off the coast of Alaska and was reportedly kept running with parts scavenged from nautical museums.

Joining the fleet is the Okeanos Explorer, which NOAA purchased from the US navy in 2004. The agency has upgraded the ship, adding two unmanned submersible vehicles, a satellite communications system for conducting experiments remotely and a fresh coat of white paint. The Okeanos Explorer

will specialize in mapping and basic exploration of interesting sites. After field testing, the vessel will head to the tropical Pacific.

Computer experts blast ruling to gag studentsComputer scientists in the United States have condemned a court order that blocks three undergraduates from the Massachusetts Institute of Technology in Cambridge from discussing aspects of their research on the security of Boston’s transit system.

The Massachusetts Bay Transportation Authority sought the order to prevent the students from giving a talk entitled “Anatomy of a Subway Hack” at a major convention in Las Vegas, Nevada. The talk exposed flaws in the transit system’s ‘smart cards’, which are used for electronic ticketing.

In a letter supporting the students, 11 leading computer scientists warn that such restraining orders “will stifle research efforts and weaken academic computing research programmes”.

As Nature went to press, a decision on whether to lift or amend the order was pending.

Plans for the largest ever solar-power plantsA utility company in the California has inked a deal for two massive solar-panel projects.

San Francisco-based Pacific Gas and Electric Company (PG&E) agreed last week to purchase power from two solar-panel manufacturers in the state. OptiSolar, based

in Hayward, will build a 550-megawatt plant, to be accompanied by a 250-megawatt plant from SunPower of San Jose.

To date, photovoltaics have been relegated to relatively small projects, measured in the tens of megawatts. PG&E’s 800-megawatt scheme would exceed the largest solar panel project in operation today by a factor of more than 30, and its power capacity could rival that of a mid-sized coal-fired power plant.

The plants are scheduled to be fully operational by 2013, but are contingent on new transmission lines and the extension of federal tax credits for renewable energy.

Science illustration course draws to an endAn award-winning science illustration programme at the University of California, Santa Cruz, is facing closure.

On 12 August, administrators announced that they would end the programme next spring because of mounting debt in the university’s continuing-education system. The 27-year-old science illustration course, one of a handful in the nation to offer graduate training, failed to bring in enough tuition dollars to cover its costs. The announced closure is the latest in a series of cuts.

The university is still looking for alternative ways to finance the illustration curriculum, says Ann Caudle, the course’s director. “There is a sliver of a chance we might continue the programme.”

New species of robin found in GabonOrnithologists from the US Smithsonian Institution have identified a tiny fiery breasted robin as a new species.

The olive-backed forest robin (Stiphrornis pyrrholaemus) was first found on an expedition to forests in southwest Gabon in 2001, but it was thought to be a juvenile of a known species. The researchers have now confirmed that the robin is a distinct species by comparing its vocalizations and genetic code with those of other specimens in the Smithsonian’s collection.

The finding was published last week in the journal Zootaxa.

CorrectionThe News Feature ‘The green menace’ (Nature 452, 148–150; 2008) failed to give the full name and affiliation of Jan Leach, a plant pathologist at Colorado State University in Fort Collins.

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The John N. Cobb has been retired after 58 years.

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