A Sentinel Plant Pathologist: Enrico Bonello

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Today’s alert focuses on Dr. Enrico Bonello, Professor in the Department of Plant Pathology Department at Ohio State University. Enrico (Pierluigi) is a member of OSU’s Extension Nursery Landscape and Turf (and Tree) Team, and I have known him since he came to OSU in 2000, but thought it was time for a profile.  Interviewing Enrico, learning “I hardly knew him”.

 

 

 

Part of the impetus for focusing on Enrico was a recent article by Gabriel Popkin in Science News (March 25), in the prestigious journal Science titled: “Scientists plant ‘sentinel trees’ to warn of devastating pests.”  

 

The basic idea for a series of Sentinel projects is to read the warning signs of potentially invasive plant  pathogens and pests by establishing research plots of plants from one part of the world in other parts of the world. Of course, botanic gardens already have plants from different continents, but not in controlled research plots to assess pest and pathogen susceptibility.

 

In retrospect, for example, if plots of North American ashes were monitored in China in the late 20th century, and had become devastated there by emerald ash borer (Agrilus planipennis) might plant and animal inspection services have been more alert to inspecting shipment of Asian ash products to North America?

 

With estimates of losses of hundreds of millions to billions of ashes and $billions from emerald ash borer killing our North American ashes, this sentinel warning system merits research resources. Multiply this for other plant/pest and pathogen interactions and you get the picture.  

 

Here is where Enrico and others enter the picture. As the Science News article notes, among a number of other projects worldwide:  “The U.S. Forest Service (USFS) is funding several projects, including one led by Ohio State University, Columbus, plant pathologist Enrico Bonello that, in April, is scheduled to plant the first sentinel trees from Asia and Europe—including beeches, hollies, maples, and pines—in Ohio and New Hampshire.”  

 

Fellow researchers on this project include Dr. Francesca Hand in the Plant Pathology Department at OSU, Dave Shetlar of the OSU Department of Entomology and Isabel Munck of the U.S. Forest Service in Durham, New Hampshire. Collaborators have already planted North American and Asian trees in Sweden and Italy.

 

So, let us take a look at the plant pathological career of Enrico Bonello. His hometown is Padua, Italy, where at the University of Padua he got his combined B.S./M.S. degree in forest sciences. He worked on cypress canker disease on Italian cypress (Cupressus sempervirens), caused by the fungus Seiridium cardinale. It is thought to be a North American pathogen, occurring on Monterey cypress, with the fungus possibly arriving in Europe on cypress ammunition boxes in World War II. 
 

This canker disease is more severe on the Italian cypresses that did not evolve in the caldron of natural selection with this foreign (to Italy) pathogen. In this we can perhaps trace Enrico’s phytopathological passion for studying mechanisms of plant resistance to pathogens.
 

The pathogen and diseases on cypress is now widespread around the globe, as indicated from this torn-from-the headlines in a different context quote from a 2017 article in  the journal Plant Disease (Published Online:15 Aug 2017https://doi.org/10.1094/PDIS-05-17-0746-PDN) by J. Della Rocca.
 

“Cypress canker is a pandemic disease of cupressaceous plants caused by Seiridium cardinale (Wagener) Sutton & Gibson, a fungus recently shown to be native to California.”
 

I encourage bygl-alert readers to spend some time in our current exile to learn about mechanisms of disease resistance, of secondary metabolites such as terpenes, about the role of natural selection. The use of terms such as “pandemic” and the roles of natural selection and the evolution of disease resistance over time are quite apropos to all of our current crash course in infectious disease biology.
 

Next, Enrico headed for Oxford (not Ohio) for his PhD work, studying basic mechanisms of resistance of Scots pine to an array of soilborne plant pathogenic fungi and oomycetes (known as water mold fungi at the time) .  Pathogens studied included Cylindrocarpon destructans and Pythium species.  Aren’t plant pathogen names wonderful?

 

Enrico’s globe-trotting then took him to Munich, and then California. In Munich at the German Research Center for Environmental Health (Helmholtz Zentrum München) he studied how the effects of ozone pollution affects Scots pine resistance/susceptibility to Heterobasidium annosum, the cause of Annosum root rot, considered to be the most damaging forest disease in the Northern Hemisphere, perhaps causing over $1 billion damage in the U.S.


 

In California, at the University of California-Berkeley, Enrico continued with his research on the mechanisms of plant disease resistance, looking at the Ponderosa pine patho-system with Heterobasidum annosum  and interactions with an insect pest, the western pine beetles, Dendroctonus brevicomis.

 


 

Then at the University of California-Davis, he studied Ponderosa pine and pitch canker, Fusarium circinatum. While at UC-Davis, Enrico first became involved in work on the oomycete pathogen, Phytophthora ramorum and Sudden Oak Death (SOD), an emerging major problem on oaks (Quercus spp.) and tanoaks (Lithocarpus spp.).
 

Diplodia tip blight of pine
Diplodia tip blight of pine. Note browning and stunting of the new growth. New shoots are above the spent male strobili.

 

You are beginning to see why OSU was interested in Enrico’s wide background in forest pathology and the forefront of research on the mechanisms of disease resistance. He started at OSU in 2000 and began researching Diplodia tip blight of Austrian pine, a major two-needled landscape pine planted extensively in Ohio and the eastern U.S.  One avenue of this research was on the emerging investigations of “systemic acquired resistance”: how does a plant react in one part of the plant when challenged with inoculation with the pathogen in another part of the plant?
 

Diplodia tip blight of pine
Diplodia tip blight of pine. Note dieback on lower branches on early years of infection.

 

Diplodia tip blight of pine
Diplodia tip blight of pine. Note the stunted, blighted needles. Notice the unsheathed needle with tiny black fruiting bodies of the fungus

 

 

Enrico also soon became re-involved with Phytophthora ramorum and SOD. The pathogen was an important regulatory problem since there was great concern that this invasive pathogen (thought to originate in Europe) and now killing tens of thousands of oaks and tanoaks in the Pacific Northwest, could become an issue in the Eastern U.S. through contaminated nursery stock. There was even a well-publicized case of a California nursery that had to destroy millions of dollars of nursery stock because a wide range of hosts were infected with Phytophthora ramorum.  

 

Sudden oak death symptoms
Sudden oak death on the West Coast. From WIkipedia


 
Some nursery plants from the West had escaped regulatory efforts and were sent Eastward. Which brings up a name issue. Rhododendrons, lilacs, camellias, California buckeye (!) and many other hosts, all are susceptible to Phytophthora ramorum (Phytophthora means “plant destroyer”, and ramorum  means “of the branches”).  This resulted in confusion.
 

The disease was called Sudden Oak Death and was a killer on oaks, but often resulted just in leaf spots and twig dieback on other hosts. This no doubt is part of why it was missed in regulatory inspections, since these other hosts were not dying.  But the disease name was Sudden Oak Death, focusing on the oak hosts.  We now encourage the use of the moniker PRAM disease or Phytophthora Ramorum Disease on, for example Rhododendron, helping make the distinction as to which host plant is affected.  
 

At any rate, with this experience, Enrico became involved here in Ohio with efforts to assess whether the disease was a problem in the eastern U.S. He soon was the coordinator of a regional lab to check for the presence of Phytophthora ramorum. To date, two decades later, the pathogen is not known to have become established in Ohio or elsewhere in the East, but it has escaped inspections of Pacific northwest nursery stock (rhododendrons, lilacs, etc.) several times including a well-publicized episode this summer in which infected West Coast nursery plants were sent to Oklahoma and then on to Ohio and other states.
 

Over the years the pathogen has been found in non-oak hosts in nurseries in the East, traced from these escapes in nursery stock shipped Eastward, with plants subsequently destroyed. There have been no known infestations of oaks in the eastern United States, presumably because we do not have the Environmental Conditions Conducive to Disease as found in the fog forests and other humid areas of the Pacific Northwest.
 

Meanwhile, Enrico has studied and published on a number of other tree diseases her in Ohio. One of these is a disease called oak decline, thought to be due to another species of Phytophthora that is common to this area, Phytophthora cinnamomi. In addition, because of his expertise in researching disease resistance mechanisms in trees, Enrico is a major partner in studying resistance to an insect, the emerald ash borer, working with entomologists Dan Herms of OSU and now the VP of research with the Davey Tree Expert Company, and Don Cipollini of Wright State University.  
 

Other projects include working again on SOD with West Coast colleagues, developing non-destructive techniques for identifying resistance in California live oak (Quercus agrifolia), working with European colleagues on resistance systems of European ashes to ash dieback there (Hymenoscyphus fraxineus) and looking at white pine blister rust (Cronartium ribicola) on one of the five-needled western U.S. pines, the ecologically important whitebarked pine (Pinus albicaulis). 
 

white pine blister rust
White pine blister rust at the Dan and Cathy Herms cabin in Michigan

 

Gotta love those Latin binomials: for example, Cronartium ribicola, of which the second part of the binomial, the specific epithet, refers to the fact that the alternate host for this rust fungus are certain species of currants and gooseberries in the genus – Ribes.
 

Enrico has continued to work on the Diplodia tip blight of pine pathosystem and many other projects, but an important new focus in his OSU lab is working with his PhD student Carrie Ewing in investigating a new disease of beeches: Beech Leaf Disease.
 

This disease, with symptoms of yellow and green banding on leaves, leaf blistering, brown leaf blotching, twig dieback and proceeding in some cases to canopy thinning and even tree death was first noticed in 2013 by biologist John Pojacnik of Ohio’s Lake (County) Metroparks. It has now been found at a number of sites in northeast Ohio, Ontario, Long Island Sound in New York, and across the waters there in Connecticut.

 

Beech leaf disease
Note the banding on American beech foliage from Beech Leaf Disease 

 

Beech leaf disease
Leaf puckering symptom of Beech Leaf Disease


 

Beech Leaf Disease
Foliar discooration and necrotic spots from Beech Leaf Disease on Long Island in New York

 

We still do not know what causes this disease, but foliar nematodes are associated with it (the Ohio Department of Agriculture was key in this observation), and many theories abound as to whether or not the disease complex includes other plant pathogens such as viruses or fungi, and eriophyid mites.  We have seen it in woodlands on American beech (Fagus grandifolia) and European and Asian beeches in nurseries. Nematodes are associated with what seems to be a similar problem on beeches in Asia. As they say on our news feeds: this is a developing story.  
 

So, plenty to whet your curiosity about one of the key international players in forest health, OSU’s Dr. Enrico Bonello. We look forward to more from the front lines of understanding mechanisms of plant disease and pest resistance, including the research in years to come from the Sentinel Project.    
 

Enrico Bonello
Enrico Bonello casts a long shadow at an OSU Extension program on oak wilt. Picnic beetles shown are vectors of the fungus that causes the oak wilt vascular wilt