MOLECULAR PLANT PATHOLOGY (2010) 11(3), 325–334 DOI: 10.1111/J.1364-3703.2010.00616.

Pathogen profile
Phymatotrichum (cotton) root rot caused by Phymatotrichopsis
omnivora: retrospects and prospects

SRINIVASA RAO UPPALAPATI 1 , CAROLYN A. YOUNG 2 , STEPHEN M. MAREK 3 AND

KIRANKUMAR S. MYSORE 1, *
1
Plant Biology Division, The Samuel Roberts Noble Foundation Inc., 2510 Sam Noble Parkway, Ardmore, OK 73401, USA
2
Forage Improvement Division, The Samuel Roberts Noble Foundation Inc., 2510 Sam Noble Parkway, Ardmore, OK 73401, USA
3
Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA

mainly colonize cortical cells and eventually form a mycelial

SUMMARY
mantle covering the root’s surfaces. Cell wall-degrading enzymes
Phymatotrichum (cotton or Texas) root rot is caused by the have been implicated in penetration and symptom development.
soil-borne fungus Phymatotrichopsis omnivora (Duggar) Hen- Global gene expression profiling of infected M. truncatula
nebert. The broad host range of the fungus includes numerous revealed roles for jasmonic acid, ethylene and the flavonoid
crop plants, such as alfalfa and cotton. Together with an over- pathway during disease development. Phymatotrichopsis
view of existing knowledge, this review is aimed at discussing omnivora apparently evades induced host defences and may
the recent molecular and genomic approaches that have been suppress the host’s phytochemical defences at later stages of
undertaken to better understand the disease development at the infection to favour pathogenesis.
molecular level with the ultimate goal of developing resistant Disease control: No consistently effective control measures
germplasm. mpp_616 325..334 are known. The long-lived sclerotia and facultative saprotro-
Taxonomy: Phymatotrichopsis omnivora (Duggar) Hennebert phism of P. omnivora make crop rotation ineffective. Chemical
[synonym Phymatotrichum omnivorum (Shear) Duggar] is an fumigation methods are not cost-effective for most crops. Inter-
asexual fungus with no known sexual stage. Mitosporic botryo- estingly, no genetic resistance has been reported in any of the
blastospores occasionally form on epigeous spore mats in susceptible crop species.
nature, but perform no known function and do not contribute to
the disease cycle. The fungus has been affiliated erroneously
with the polypore basidiomycete Sistotrema brinkmannii (Bres.)
J. Erikss. Recent phylogenetic studies have placed this fungus in INTRODUCTION
the ascomycete order Pezizales. Phymatotrichum root rot (PRR) is one of the most destructive
Host range and disease symptoms: The fungus infects diseases of cotton (Gossypium spp.) and alfalfa (Medicago
most dicotyledonous field crops, causing significant losses to sativa), the most important source of natural fibre and one of the
cotton, alfalfa, grape, fruit and nut trees and ornamental shrubs in most important forage crops, respectively. Alfalfa is the fourth
the south-western USA, northern Mexico and possibly parts of most widely grown crop in the USA and is valued at more than 40
central Asia. However, this fungus does not cause disease in million dollars annually (http://www.naaic.org). PRR causes sig-
monocotyledonous plants. Symptoms include an expanding nificant economic losses every year in the USA. Duggar (1916)
tissue collapse (rot) of infected taproots. In above-ground tissues, named the causal fungus Phymatotrichum omnivorum (Shear)
the root rot results in vascular discoloration of the stem and rapid Duggar on the basis of observations of botryoblastosporic conid-
wilting of the leaves without abscission, and eventually the death iophores produced on spore mats. However, Hennebert (1973)
of the plant. Characteristic mycelial strands of the pathogen are renamed the fungus as Phymatotrichopsis omnivora (Duggar)
typically present on the root’s surface, aiding diagnosis. Hennebert to correct the invalid genus name Phymatotrichum,
Pathogenicity: Confocal imaging of P. omnivora interactions whilst emphasizing its morphological affinity to Botrytis-like
with Medicago truncatula roots revealed that infecting hyphae Ascomycetes.
do not form any specialized structures for penetration and Phymatotrichopsis omnivora has a very broad host range and
attacks almost 2000 dicotyledonous species, but interestingly is
*Correspondence: E-mail: ksmysore@noble.org not known to affect monocotyledonous species, including maize

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and sorghum (Taubenhaus and Ezekiel, 1936). In addition, the constructed, P. omnivora is a member of the class Pezizomycetes
disease only occurs in plants growing in alkaline, calcareous soils (‘operculate discomycetes’) within the Ascomycota and belongs
that rarely freeze deeply. Therefore, the geographical distribution to the formerly monotypic family Rhizinaceae (Fig. 1). Previously,
of the fungus is mainly restricted to the south-western USA and only three genera in the Pezizomycetes were known to be plant
northern Mexico (Percy, 1983). A similar soil-borne disease pathogens, Rhizina, Caloscypha and Strumella, and the majority
occurs in central Asia (Mishra, 1953) and the causal fungus, of species in this class are believed to possess saprobic or myc-
Ozonium texanum Neal and Wester. var. parasiticum Thirumala- orrhizal lifestyles (Hansen and Pfister, 2006; Tedersoo et al.,
char (Neal and Wester, 1934; Thirumalachar, 1951), may be syn- 2006). Placement of P. omnivora in the Rhizinaceae seems
onymous with P. omnivora, but molecular confirmation is appropriate, as another member of this family, Rhizina undulata
lacking. Fr., causes a similar disease, Rhizina root rot, of pine seedlings
Since the first report of this pathogen by Pammel (1888), and produces similar hypogeous mycelial strands that cover
various researchers have studied the biology, epidemiology and infected roots (Booth and Gibson, 1998). However, R. undulata
control (chemical, biological and genetic) of this disease. readily forms long-lived ascospores in apothecia, whereas P.
Although several management practices have been used to help omnivora occasionally forms short-lived conidia on spore mats. A
reduce the occurrence and severity of this disease, none are better understanding of the diseases caused by the other patho-
cost-effective and PRR remains one of the most destructive genic Pezizomycetes would provide a crucial evolutionary
pathogens affecting many economically important field crops context for PRR research and a platform for future comparative
and tree species. Previous reviews (Lyda, 1978; Lyda and Kener- genomics studies.
ley, 1993) and a monograph on PRR (Streets and Bloss, 1973) During its life cycle (Fig. 2), the fungus forms several differen-
present a detailed overview of the epidemiology and plant tiated hyphae. Initial hyphae produced from the primary inocu-
disease management strategies. Despite the extensive research lum, hypogeous sclerotia, consist of septate, large-diameter (10–
performed on this fungus over the past 100 years, several areas 20 mm), multinucleate cells, with right-angled branch cells that
of the physiological and molecular plant–microbe interactions resemble those of Rhizoctonia spp. (Fig. 3a; Dong et al., 1981;
remain poorly understood. In this review, we present a brief Hosford and Gries, 1966). Thin (~5 mm) runner hyphae wrap
overview of the research conducted to date and discuss the around the large central hypha, interweaving into a multilayered
prospects of utilizing functional genomic approaches to further mycelial strand (Fig. 3b; Alderman and Stowell, 1986). Mycelia
elucidate the processes of the PRR pathosystem. also form strands when cultured on nutritionally poor media
(Alderman and Stowell, 1986). Characteristic acicular hyphae
project perpendicular from the rhizomorph-like strands, forming
TAXONOMY AND LIFE CYCLE
cruciform branches that are used to identify the fungus (Fig. 3b).
The soil-borne, filamentous P. omnivora has no known sexual The mycelial strands grow through soil along roots, disseminat-
stage (teleomorph). Pammel (1888) identified P. omnivora as ing the infection from root to root (Fig. 2). The role of the myce-
Ozonium auricomum Lk. Later, Shear (1907) changed the species lial strands in the life of this pathogen, both as inoculum and
to Ozonium omnivorum based on its parasitic lifestyle and dif- survival structures, has been a subject of debate. However, Alder-
ferences in mycelial morphology from the type culture of O. man and Hine (1982) concluded that strands are formed in large
auricomum. In fact, the disease was (and is sometimes still) numbers during disease occurrence, but cannot act as primary
referred to as Ozonium root rot by some authors. On identifica- inoculum and incite disease.
tion of the conidial stage on spore mats, Duggar (1916) renamed Mycelial strands growing away from a nutrient source form
the PRR fungus Phymatotrichum omnivorum (Shear) Duggar. The sclerotia that can survive for several years in the absence of the
rhizomorph-like mycelial strands and the observation of polypor- host (Rogers, 1942) and serve as the primary survival propagules
oid basidiomata on PRR-infected plants have led to the misiden- in the field (Neal, 1929). Earlier studies on P. omnivora have
tification of the sexual stage as Hydnum omnivorum (Shear, focused on understanding the nutritional and edaphic require-
1925) and Sistotrema brinkmannii (Bref.) J. Erikss. (Baniecki and ments controlling sclerotial production, distribution and germi-
Bloss, 1969), but these were subsequently refuted (Dong et al., nation in the field (Gunasekaran and Webber, 1974; Kenerley and
1981; Weresub and Leclair, 1971). Finally, the fungus was Stack, 1987; Kenerley et al., 1998; see review by Lyda, 1978).
renamed Phymatotrichopsis omnivora (Duggar) Hennebert Sclerotia can be cultured in the laboratory in Houston black clay
(1973) to reassert its mitosporic affinity to Botrytis-like overlain with a suitable nutrient source, such as sterilized
species. sorghum or wheat grains (Dunlap, 1941; Lyda and Kenerley,
Recently, the molecular systematics of P. omnivora have been 1992; Fig. 3c). Depending on the strain, strands of P. omnivora
determined using the ribosomal DNA and RNA polymerase II rapidly colonize the soil in 2 weeks. After 4–6 weeks, strand cells
subunit 2 loci (Marek et al., 2009). According to the phylogenies divide, grow and enlarge to form sclerotia (Fig. 3d). The sclerotia

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 Phymatotrichum root rot 327

Fig. 1 Multilocus phylogenetic placement of Phymatotrichopsis omnivora. The tree on the left shows P. omnivora’s placement among the classes of the
Ascomycota and its relationship to other plant pathogenic species, for which genome sequences are available (based on Hibbett et al., 2007). The tree on the
right shows the placement of P. omnivora within the family Rhizinaceae and its relationship to other families and plant pathogenic genera (asterisks) among
the three lineages of the Pezizomycetes (based on Marek et al., 2009).

Fig. 2 Soil-borne disease cycle of

Phymatotrichum root rot (adapted from Charles
Kenerley, personal communication).

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Fig. 3 Morphology, symptoms and signs of Phymatotrichum root rot (PRR): (a) multinucleate large hypha stained with propidium iodide (¥400); (b) acicular and
cruciform hyphae (arrows) on mycelial strand (¥50); (c) Magenta box soil culture for sclerotia production; (d) sclerotia (arrow) forming along mycelial strands
(arrowhead); (e) sclerotia wet sieved from soil cultures; (f) sclerotium germinating on defined agar medium; (g) nascent mycelial strands (arrows) of
Phymatotrichopsis omnivora colonizing the surface of an asymptomatic cotton root; (h) spore mat on soil surface near infection focus in alfalfa field; (i) ‘fairy
ring’-like disease foci in an alfalfa field; (j) circular disease foci in defoliated cotton field showing the yield loss; (k) cotton plant killed by PRR (arrow) adjacent
to wilting plants succumbing to PRR; (l) vascular discoloration of PRR-wilted cotton plant; (m) cortical lesions on cotton root (epidermis removed); (n) mature
mycelial strands (arrowhead) of P. omnivora on the root of a wilted cotton plant.

are irregular in shape and become brown with age (Fig. 3e). (Fig. 3g). Individual hyphae penetrate the host root tissue initi-
Sclerotia can be stored in a refrigerator for several weeks, can be ating the disease. The strands formed on root surfaces then form
germinated in defined media (Fig. 3f) and soil, and can serve as sclerotia in the surrounding soil, thus completing the life cycle
a primary inoculum for laboratory experiments. Germ tubes (Fig. 2).
erupting from sclerotia eventually form mycelial strands and, on After periods of rain, P. omnivora forms spore mats on the soil
contact with root cells, form a hyphal mantle on the root surface surface at the margins of PRR infection foci in the field (Fig. 3h).

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The conidial stage of P. omnivora is abundantly produced on the

IN VITRO AND IN PLANTA PATHOGEN
surface of these spore mats (Duggar, 1916; Hosford and Gries,
PHYSIOLOGY
1966). To date, the germination of conidia has rarely been
observed and the role of conidia in the life cycle of this pathogen Many previous researchers have attempted to understand the
remains a mystery. nutritional requirements and metabolic pathways of P. omnivora
in order to gain a better insight into its broad host range. In
general, P. omnivora can utilize monosaccharides, disaccharides
GEOGRAPHICAL DISTRIBUTION, HOST RANGE,
or polysaccharides as carbon sources (Ezekiel et al., 1934;
DISEASE SYMPTOMS AND DIAGNOSIS
Gunasekaran, 1973). Gunasekaran (1973, 1980) reported bio-
Phymatotrichopsis omnivora is widespread in the alkaline, cal- chemical evidence for the presence of carbon catabolic pathways
careous soils of the south-western USA (Oklahoma, Texas, New and amylase activity. P. omnivora also grows well on chemically
Mexico and Arizona) and northern Mexico (Percy, 1983), and defined media supplemented with micronutrients (Ezekiel, 1945;
possibly India and Pakistan (Lyda, 1972; Mishra, 1953). More Talley and Blank, 1941). Although, in nature, it is confined to
than 2000 dicotyledonous species are susceptible to various alkaline soils, the fungus grows well over a wide range of pH
degrees to P. omnivora (Streets, 1937; Taubenhaus and Ezekiel, values in vitro (Gunasekaran, 1973).
1936). The wide host range of this fungus has made disease The formation of mycelial strands and sclerotia is important
management through crop rotation ineffective. When endemic, for the successful colonization of new host roots and for survival,
PRR causes significant economical losses on many field crops, respectively. Strand and sclerotial formation are favoured by
such as cotton, alfalfa and peanuts. PRR can also cause losses on nutrient depletion and low moisture, whereas potassium- and
horticultural crops, such as pecans, apples and ornamental trees phosphorus-enriched growth media inhibit strand formation
and shrubs. The fungus is prevalent throughout much of the (Bloss and Wheeler, 1975; Kenerley et al., 1998). During morpho-
cotton-growing area of Texas, and so the disease is also called genesis, sclerotial cells synthesize and store copious amounts of
‘cotton root rot’ or ‘Texas root rot’. PRR causes an average of glycogen, which accumulates to over 30% of the total dry weight
$100 million in annual losses to the US cotton crop alone (based (Ergle, 1947). Most of the nuclei of sclerotial cells enter a con-
on disease loss estimates and price data for 1980–2008; pro- densed resting state (G0) in which the DNA is methylated
vided by the National Cotton Council of America, http:// (Hosford and Gries, 1966; Jupe et al., 1986). On germination,
www.cotton.org). most of the glycogen in the sclerotia is catabolized (Ergle, 1948)
PRR can also cause significant economic losses to alfalfa and nuclei appear to divide rapidly and move into hyphal cells
(lucerne, Medicago sativa L.) by reducing the productivity and emerging from the sclerotia (Hosford and Gries, 1966).
persistence of hay fields. PRR of alfalfa has been much less Extensive cytological and biochemical research has been con-
studied than PRR of cotton. However, it is important to note ducted to better understand the process of penetration and the
that disease progression and symptoms are very similar in invasion of cotton root tissues by P. omnivora (Watkins, 1938a,
cotton and alfalfa fields (Fig. 3g–n), even though alfalfa is b; Watkins and Watkins, 1940). These previous studies have
grown as a perennial. At the field level, the disease mainly suggested the involvement of mechanical pressure and secreted
occurs as circular infection foci of dead plants in alfalfa (Fig. 3i) cell wall hydrolases during the penetration and colonization
and cotton (Fig. 3j), which expand over the summer. The myce- of host roots. Infectious hyphae penetrate the root tissues
lial strands (Fig. 3b,g,n) formed on the roots of plants at the necrotrophically, with host cells collapsing in advance of hyphae,
periphery of infection foci permit P. omnivora to radiate out- until the vascular bundle is reached. Similarly, thermolabile sub-
wards through the soil until it comes into contact with a new stances, presumably enzymes, isolated from infected cotton
host root. The strands envelop roots and young hyphae can roots and hyphae cause dramatic necrosis of cotton seedling
directly penetrate and form infection cushions on the host roots (Watkins and Watkins, 1940). When supplemented with the
tissue. Hyphae grow both intra- and intercellularly and pen- appropriate carbon source, P. omnivora secretes cellobiohydro-
etrate to the endodermis and xylem tissue (Watkins, 1938a, b). lase, endoglucanase and xylanase enzymes in culture (Ortega,
In cotton fields, symptoms are most conspicuous during the 1995). In addition, during P. omnivora infection of cotton, pectin
summer when the infected plants suddenly wilt (Fig. 3k). The transeliminase, polygalacturonase, cellulase, amylase and
roots at this stage show extensive vascular discoloration polyphenoloxidase activities increase over the first 2 weeks post-
(Fig. 3l) and the cortical lesions can be easily visualized after inoculation (Castrejón Sanguino et al., 1984). P. omnivora is also
removal of the periderm (Fig. 3m). As the disease progresses, known to produce several phenolics in culture (Gunasekaran,
the dead roots are extensively colonized by mycelial strands 1982), including a high-molecular-weight phenolic protein
(Fig. 3n), which is one of the typical characteristic symptoms of complex produced by the fungus in planta. It has also been
PRR. shown that the phenolic protein complex produced in culture

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can induce wilting on application to cotton seedlings (Misaghi erance against PRR. However, relative tolerance to PRR was
and Cotty, 1993). observed in some genotypes of cotton (MLB2BENH-1-85) that
There is very limited information on the host response during showed less incidence of disease (Cook and El-Zik, 1991). More
pathogenesis or on the physiological and biochemical aspects of recently, work has begun on the screening of alfalfa and Medi-
the interaction. A range of phenolic compounds are present in cago truncatula ecotypes for resistance. A growth chamber assay
plants that are toxic to the fungus in vitro (Greathouse and has been developed but, to date, no clear resistant varieties have
Rigler, 1940). However, Greathouse and Rigler (1940) presented been identified (S.R. Uppalapati and K.S. Mysore, unpublished;
no evidence for the pathogen-induced phenolics or other phy- C.A. Young and H.-K. Lee, unpublished).
toalexins or their role in restricting fungal growth.

FUTURE PROSPECTS: FUNCTIONAL GENOMIC

EPIDEMIOLOGY AND CONTROL OF PRR APPROACHES FOR THE STUDY OF PRR
Lyda and Kenerley (1993) have presented a comprehensive his- To date, little information is available at the biochemical and
torical prospective on the control and management of PRR. molecular levels on the pathogenicity/virulence factors that are
Various approaches, such as deep tillage, subsoiling with dyna- important to disease development. Some new insights based on
mite, flooding and root barriers, have been implemented and recent research into the molecular characterization of this patho-
have been found to facilitate or impede pathogen dissemination. system are presented below.
A wide range of chemical control measures have also been
tested with even less success; however, methyl bromide (Lyda
Molecular basis of P. omnivora–host interactions
et al., 1967), anhydrous ammonia and ammonium salts (Neal
et al., 1933; Rush and Lyda, 1984) have been found to be effec- The relative genetic intractability of cotton and alfalfa (M. sativa)
tive. However, large quantities of these chemicals must be as pathosystem hosts for P. omnivora precludes most genomic
injected deeply into the soil, making it expensive and therefore approaches. Recently, we employed the close relative of alfalfa
not commercially feasible. Although the application of systemic and the model legume, Medicago truncatula, as a pathosystem
fungicides, such as benzimidazoles and sterol biosynthesis to investigate the cellular and molecular events during P.
inhibitors, has been shown to reduce the incidence of PRR omnivora infection (Uppalapati et al., 2009). Unlike alfalfa,
(Matheison and Lyda, 1984; Whitson and Hine, 1986), there are which is a tetraploid and obligate outcrossing species, M. trun-
no systemic fungicides labelled for P. omnivora. However, as catula has a simple diploid genome (two sets of eight chromo-
most systemic fungicides are relatively expensive, exhibit poor somes) and can be self-pollinated. M. truncatula is fast emerging
basipetal translocation to the roots, and poor persistence and as a model legume because of its small genome, which is almost
penetration in the soil, the efficacy of these products should be completely sequenced (Young et al., 2005), fast generation time,
evaluated carefully. high transformation efficiency and the availability of Affymetrix
Reduced PRR in fields fertilized with manure and the per- gene chips, numerous ecotypes, and ethyl methyl sulfonate, fast-
ceived resistance of monocots have both been attributed to neutron and insertional mutants (Tadege et al., 2005; Zhu et al.,
increased microbial competition (Eaton and Rigler, 1946; Streets, 2005). Phymatotrichopsis omnivora causes typical PRR disease
1937). Several fungal antagonists of P. omnivora in the genera symptoms on M. truncatula (Fig. 4a, Uppalapati et al., 2009). The
Gliocladium and Trichoderma have been suggested as candidate development of leaf chlorosis and vascular discoloration
biological control agents (Kenerley and Stack, 1987; Kenerley (Fig. 4b) suggests that P. omnivora produces a translocated phy-
et al., 1987; Taubenhaus and Ezekiel, 1933). Although these totoxin. Infected M. truncatula roots show browning and typical
fungi colonized the sclerotia of P. omnivora, no satisfactory necrotic lesions at the site of hyphal penetration (Fig. 4a). Cyto-
control of PRR has been reported with applications of these logical observations of the interaction using light and confocal
mycoparasites. laser scanning microscopy (CLSM) of the fungal mycelia follow-
Ideally, the identification of PRR-resistant host germplasm for ing immunostaining with Alexa Fluor 488 revealed that, on
plant breeding would be the optimal approach for the manage- contact, hyphae grew parallel along the longitudinal groove
ment of this disease (Bird et al., 1977, 1980; Blank, 1940; Cook between the root’s epidermal cells, and then grew perpendicu-
and El-Zik, 1991; Percy and Rush, 1985). Initial screens for resis- larly and centripetally into the junctions between the epidermal
tance to PRR identified cotton genotypes with reduced mortality, cells (Fig. 4c; Uppalapati et al., 2009). Furthermore, we observed
but did not result in the release of a resistant variety (Goldsmith that the nuclei of plant epidermal cells were located adjacent to
and Moore, 1941). Percy and Rush (1985) evaluated four upland the cell wall proximal to the hyphal tips (Uppalapati et al., 2009).
cotton genotypes for rate-limiting resistance under controlled It is not clear whether nuclear repositioning leads to the forma-
conditions and observed no evidence of host resistance or tol- tion of pre-penetration apparatuses, as in arbuscular mycorrhizal

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Fig. 4 Symptom development and stages of

Medicago truncatula root colonization by
Phymatotrichopsis omnivora: (a) Phymatotrichum
root rot symptom and necrotic lesion
development; (b) overhead view of M. truncatula
seedlings grown in tissue culture containers
inoculated with a wheat seed colonized by P.
omnivora; (c) confocal fluorescence images of
WGA-Alexa Fluor 488-stained fungal hyphae
showing colonization and entry of hyphae
between the junctions of epidermal cells (arrow),
3 days post-inoculation (dpi); (d) root sections
showing WGA-Alexa Fluor 488-stained fungal
mycelia growing in the intracellular spaces of the
cortical cells, 5 dpi. Plant cell walls were stained
with calcofluor white. Scale bars, 50 mm.

interactions (Genre et al., 2005), or whether it provides any clues defences at later stages of infection (Uppalapati et al., 2009).
for hyphal positioning or penetration. No specialized penetration Detoxification or modification of phytoalexins has been linked to
structures, such as appressoria, were revealed by CLSM. It virulence or pathogenicity in many pathosystems (Pedras and
appears that the fungus penetrates the roots directly with simple Ahiahonu, 2005; VanEtten et al., 1989). In addition, suppression
infection hyphae that branch perpendicularly from the longitu- of phytoalexin defence by a virulence factor has been shown to
dinal hyphae, covering the root’s epidermis (Fig. 4c). Intercellular be a mechanism used by Mycosphaerella pinodes to successfully
hyphae infected both epidermal and cortical cells of M. trunca- infect pea plants (Uppalapati et al., 2004). Therefore, P.
tula roots 5 days post-inoculation (dpi; Fig. 4d; Uppalapati et al., omnivora is likely to produce effector(s) that negatively regulate
2009). phytoalexin biosynthesis in alfalfa. The ongoing genome
To identify host signalling pathways triggered by P. omnivora sequencing project of P. omnivora (http://www.genome.ou.edu/
infection, we utilized microarrays to monitor the expression pro- fungi.html) might identify candidate genes involved in the
files and molecular processes associated with initial entry (3 dpi) detoxification, modification or suppression of isoflavonoid bio-
and colonization (5 dpi). Expression profiling of M. truncatula synthesis. Furthermore, the availability of alfalfa or cotton plants
roots infected by P. omnivora identified several upregulated with increased isoflavonoid contents would facilitate investiga-
genes, including the pathogenesis-related Class I and Class IV tions into the determination of whether these compounds play
chitinases and genes involved in reactive oxygen species (ROS) any role in defence against P. omnivora.
generation and phytohormone (jasmonic acid and ethylene) sig-
nalling (Uppalapati et al., 2009). These results suggested that
Molecular characterization of P. omnivora and the
ROS, in conjunction with P. omnivora-induced ethylene, play a
PRR pathosystem
role in the development of necrotic symptoms.
Interestingly, the genes involved in the early steps of phenyl- Genomic resources for compatible hosts, such as those available
propanoid metabolism (e.g. PAL, 4CL, CHS, CHR and CHI) were for M. truncatula, have allowed us to examine rapidly the plant
induced during both early and later stages of infection. In con- interaction with the pathogen. Unfortunately, the resources for
trast, the genes involved in isoflavonoid and dihydroflavonol P. omnivora are not so advanced. Many attempts have been
biosynthesis (IFS, IFR, FS, isoflavonoid glucosyltransferase, F3H) made to genetically modify P. omnivora using traditional trans-
were induced only during the early stage of infection, and then formation techniques (Yelton et al., 1984). Although we have
declined to the levels of mock-inoculated control plants at the been able to generate protoplasts from multiple isolates of this
later stage of infection, suggesting that P. omnivora apparently organism, they are nonviable (C.A. Young and S.M. Marek,
evades induced host defences and may suppress (iso)flavonoid unpublished data). Similar approaches using microprojectile

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bombardment or Agrobacterium-mediated transformation, include catalases, glycogen metabolic enzymes, protein kinases,
which are successful for many fungal species, have also failed to phosphatases and DNA repair enzymes. In phase two of the P.
result in viable transformants (S.M. Marek, unpublished data). It omnivora genome project, additional sequence data will be used
is unclear why P. omnivora is intractable to genetic manipula- to join gaps in the genome, reduce the number of contigs and
tion. The multinucleate nature of the fungus and its lack of a build super-contig scaffolds. In addition, further refinement of
viable uninucleate stage probably impede the full expression of EST annotations will better define the transcriptome from the
selectable transgenes and the purification of homokaryotic multiple developmental and pathogenic phases of P. omnivora’s
transformants. Very few members of the Pezizomycetes are life cycle.
reported to have been transformed routinely or stably (Faugeron In conclusion, the functional analysis of the genes identified in
et al., 1989; Grimaldi et al., 2005). P. omnivora–host interactions at the biochemical and molecular
The whole-genome and expressed sequence tag (EST) levels, and the integration of recent ‘omic’ approaches with
sequencing of P. omnivora have been initiated and might help to traditional physiology and biochemistry, should provide new
answer some of the following questions: Does P. omnivora insights into this century-old disease, and help with the devel-
produce yet unidentified nonspecific phytotoxins that permit the opment of improved management strategies and resistant
broad host range of this pathogen? What are the pathogenicity germplasm.
determinants? What are the regulatory and developmental cues
stimulating the formation and germination of the sclerotia?
Numerous EST libraries from P. omnivora during sclerotial devel- ACKNOWLEDGEMENTS
opment, nutrient starvation and exposure to root exudates from We thank Drs Ajith Anand for critical reading of the manuscript,
host and nonhost plants have been constructed and sequenced Hee-Kyung Lee for Fig. 3h, Charles Kenerley for sharing his expe-
(Macmil, 2009). riences, and Bruce Roe and Simone Macmil for sharing unpub-
Using a high-throughput pyrosequencing protocol (Margulies lished results. We also thank Bharat Joshi, Hee-Kyung Lee and
et al., 2005), approximately 10-fold shotgun sequence coverage Cindy Crane for technical support. This work was supported by
has been attained and is believed to represent over 99% of the the Noble Foundation and by a grant from the Consortium for
genome of P. omnivora OKAlf8 strain. Paired-end and BAC Legume Research from the Oklahoma State Regents for Higher
pyrosequencing and Sanger sequencing of shotgun and cDNA Education. S.M.M. acknowledges support from the Oklahoma
Agricultural Experiment Station (Project OK02536), the Okla-
clones are being performed to join, order and orient the genomic
homa Department of Agriculture, Food and Forestry, and Okla-
sequence data which is now fragmented across approximately homa Experimental Program to Stimulate Competitive Research.
168 000 contigs. On the basis of these sequence data, the genome S.M.M. would like to thank Madhavi Dhulipala, James N. Enis,
size was estimated to be approximately 74 Mbp, originally Sandrine Casanova, Tim Samuels, Ian Moncrief and Carrie Smith
thought to be as three haploid copies of approximately for technical assistance.
25–30 Mbp present as heterokaryotic nuclei. However, recent size
estimates based on pulsed field gel electrophoresis and hybrid-
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