Fungi
play significant ecological and economic roles. They can break down
organic matter, cause devastating agricultural blights, enter into
symbiotic relationships to protect and nourish plants, or offer a tasty
repast. For industrial applications, fungi provide a source of enzymes
to catalyze such processes as generating biofuels from plant biomass.
One large fungal group with such enzymes are the rust plant pathogens
which cannot survive on their own so they use crops as hosts, leading to
reduced yields and potentially hindering efforts to grow biomass for
fuel. Factors that could reduce the growth of plant biomass, thus
reducing biofuel production, are a target for investigation of the
Department of Energy (DOE) Joint Genome Institute (JGI).
Published the week of May 2, 2011 in the early edition of the Proceedings of the National Academy of Sciences,
the work of an international team of researchers that included Fungal
Genome Program head Igor Grigoriev, as well as several members from the
DOE JGI, compared the genomes of two rust fungi to identify the
characteristics by which these pathogens can invade their plant hosts
and to develop methods of controlling the damage they can cause. The
team led by co-first author Sebastien Duplessis of the French national
agricultural research institute (INRA) worked on the poplar leaf rust
fungus while a team led by co-first author Christina Cuomo of the Broad
Institute of MIT and Harvard and Les Szabo from Agricultural Research
Service USDA and University of Minnesota worked separately on the wheat
and Barley stem rust fungus. The two-genome consortia joined their
efforts to compare the genomic features of the two rust pathogens to
reveal the role they play in infecting the host plant and acquiring
nutrients.
Sequenced
at the DOE JGI using the Sanger platform under the 2006 Community
Sequencing Program, the 101-million base pair genome of Melampsora
larici-populina, the first tree pathogen sequenced, was made publicly
available in 2008. Poplar leaf rust outbreaks weaken poplar trees, a
candidate bioenergy feedstock whose genome sequence was published by the
DOE JGI in 2007. In this study Melampsora larici-populina was compared
with the wheat stem rust fungus sequenced by the Broad Institute. This
rust fungus causes major epidemics of both barley and wheat worldwide. A
strain known as Ug99 has spread across Africa and into Central Asia,
and overcome most of the stem rust resistant wheat varieties developed
over the past 50 years. This is first joint fungal genomics study for
the DOE JGI and the Broad Institute.
Sebastien
Duplessis said that unlike wheat and other plants, it is difficult to
estimate the economic damage resulting from poplar rust outbreaks though
the most common figure indicates as much as 50 percent annual growth
loss in poplar plantations following major rust epidemics. Part of the
problem lies in the fungal method of attack. “For a perennial species
such as poplar attacked by an obligate biotroph, the host is maintained
alive and the tree is not killed,” he said.
DOE
JGI’s Grigoriev noted that poplar rust and the wheat rust fungi are
distantly related and show genome specific expansions in gene families.
NRA’s Francis Martin, a senior author on the study and long-time DOE JGI
collaborator, said that the work means researchers now have the genomes
of two fungi that interact with poplar in very different ways. Martin
and his colleagues were part of the group that worked on the symbiont
Laccaria bicolor, whose genome sequence was published in 2008. “[The
Melampsora genome] will allow a better understanding on how a
‘bioenergy’ tree interacts with its cortege of microbial associates,” he
said. Grigoriev echoed Martin’s comments about the benefits of having
the genome sequences. “Learning how these all impact each other helps us
to grow poplar and other crops for bioenergy production,” he said.
Still,
one of the goals of the project is to be able to determine how to
disrupt the effectors by which the fungus can suppress host defense and
recognition. In the paper, the team describes a two-pronged attack where
the fungi mask their proximity to the plant and then use enzymes to
attach the fungal cell wall to the plant cell wall and then invade the
host.
“The
precise analysis of these effectors, their localization and their
targets in the host plant, and how they evolve to overcome plant
resistances will contribute to the selection and management of
sustainable resistances of poplar trees to the rust disease,” said
Duplessis.
He
said the researchers plan to sequence more Melampsora genomes to better
understand the process by which the rust fungus adapts to its host and
overcome the plant’s resistance. “Our paper demonstrates that the rust
fungi genomes contain more than a thousand of such small effectors that
likely interfere with plant perception systems and activation of defense
reactions. Thus a targeted approach to disrupt the effectors entry and
action might be complicated. However, sequencing the rust fungus genome
opens great perspectives to study the evolution of these candidate
effectors and further define new resistances through breeding strategies
in tree plantations.”
“With
these blueprints we can then go and analyze at a population biology
level the genetic diversity of pathogens as they evolve and adapt to
control agents such as fungicides to develop more coordinated management
strategies,” said Pietro Spanu, a molecular plant biologist at Imperial
College London who studies a mildew that is also a fungal pathogen.
“The genome sequences are really toolkits,” he said. “They give us lots
of information on how the organisms evolved, allowing us to make
hypotheses on what fungi need to become obligate parasites.”
Spanu
also said that the paper is part of a recent spate in genome
publications on these fungi, and the information allows researchers to
see for the first time the “remarkable convergences” in the evolution of
these pathogens. “It’s like discovering that in order to fly you need
wings, and each group has different types of wings.”