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Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
Frances Trail 1
Departments of Plant Biology and Plant Pathology, Michigan State University, East Lansing, Michigan 48824
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ABSTRACT |
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Worldwide, one of the most devastating pathogens of small grains is the head blight fungus, Gibberella zeae. Ascospore-laden perithecia of this fungus develop on mature cereal crops and crop debris and provide the primary inoculum of the disease. We characterize the process of colonization of wheat tissue that leads to perithecium production. Stems were colonized systemically and extensively following inoculation of the wheat head. Haploid mycelia moved down the vascular system and pith and then colonized the stem tissue radially. Dikaryotic hyphae developed at two distinct stages: in the xylem, in support of radial hyphal growth and in the chloremchyma, in support of perithecium development. Perithecium formation was initiated in association with stomates and silica cells. Vascular occlusions prevented mycelia from colonizing the stem in 25% of inoculated plants. Implications of these findings are discussed for developing resistant cultivars and improving chemical control of the disease.
Key words: Ascospores, dikaryotic hyphae, perithecia, stomates, vascular occlusions
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The trichothecene deoxynivalenol, a potent protein bio-synthesis inhibitor and zearalenone, an estrogenic mycotoxin, are found in grains after FHB epidemics in North America (Neish et al 1982, Seaman 1982). Zearalenone and deoxynivalenol have been linked to feed refusal and toxicoses in livestock and present a threat to human safety (Forsyth et al 1977, Vesonder and Hesseltine 1981). Limited control of this disease can be achieved through fungicide applications, resistance breeding and crop rotation in conjunction with proper tillage (Bai and Shaner 1994).
G. zeae is a homothallic fungus capable of outcrossing. The genetic basis of homothallism recently has been described and resides in the MAT loci (Lee et al 2003). Airborne ascospores are thought to be the primary inoculum for FHB (Shaner 2003) and this, in combination with the homothallic nature of the fungus, makes the study of sexual spore production feasible and important. The epidemiology and development of FHB has been studied best in wheat (Sutton 1982, Parry et al 1995), although corn debris is probably the major source of ascospore inoculum in corn-growing regions of the U.S. (reviewed by Shaner 2003). In G. zeae, ascospores are formed in ephemeral perithecia during periods of milder temperatures and moist conditions (Khonga and Sutton 1988, Fernandez and Fernandes 1990, Reis 1990) and are discharged forcibly into the air when mature. The spores are transported on the wind and infect wheat spikelets during anthesis, when the florets are most susceptible (Pugh et al 1933).
Symptoms begin to appear at the point of infection in the form of water-soaked brown spots and eventually spread up and down the rachis. Bleaching is a common symptom of this disease and can be seen clearly on wheat heads before senescence (Parry et al 1995). Ample colonization of wheat tissue is important to pathogen survival and several studies have addressed this process. G. zeae colonized wheat stem bases, but infections that were initiated at the stem base failed to reach the head (Clement and Parry 1998). Other studies have shown that G. zeae hyphae directly penetrate ovaries, glumes and inner walls of the palea and lemma (Tu 1953, Pugh et al 1933, Pritsch et al 2000, Wanyoike et al 2002, Bushnell et al 2003). Furthermore, symptoms progress down the stem from head infections (Strausbaugh and Maloy 1986). However, these reports did not investigate the process of mycelial differentiation and stem colonization leading to perithecium development. Extensive colonization of wheat stems after head infections greatly increases the potential for inoculum production and survival of G. zeae in the field, as these tissues remain intact through the winter and serve as the basis for inoculum production in the spring (Dill-Macky and Jones 2000). A review of stem anatomy is presented in FIG. 1. Esau (1953) has described the arrangement of cell types that defines each of these plant parts.
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), our goal was to establish a system to investigate in planta differentiation leading to sexual development of G. zeae. When compared to head tissues, stem tissues provide a simpler system for examining the plant-fungus interface using functional genomics and the work presented here will serve as the basis for those investigations. As presented, our findings suggest that the downward colonization of wheat stems is extensive and that specific host tissues are preferential for colonization and perithecium development by G. zeae. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Wheat cultivar and inoculation of plants.— – Seeds of spring wheat (Triticum aestivum L.) cv. Norm were planted in 9 cm clay pots in a greenhouse designated to contain transgenic microbes and maintained at approximately 24 C with supplemental lighting. Plants were inoculated 3–4 d before anthesis by pipetting 10 µL of conidial suspension into a spikelet at the midpoint of the rachis. Plants then were placed in a mist chamber at 24 C for 4 d, before being returned to the greenhouse. Symptoms were observed daily after mist chamber treatments. Starting at 12 d after inoculation (dai), individual plants were harvested for microscopic examination.
Localization of infection front.— – Greenhouse-inoculated plants were prepared as follows. Heads were cut from each plant immediately below the lowest spikelet and the remaining stem was sectioned into 5 cm pieces. For each piece, freehand sections were removed from both ends with a razor blade. These were mounted in distilled water and immediately observed microscopically. If the sections from the distal end exhibited no fungal infection and the sections from the proximal end showed infection, the piece was cut into 1 cm segments and freehand sections from the ends of each segment were examined microscopically to locate the infection front. Sixty-five stems were analyzed in this manner. Regression analysis was performed on data representing the length of stem colonized below wheat heads, for all observed plants, using Sigmaplot 2000.
Determination of the presence of vascular gels.— –
The vessels of freehand sections from wheat stems initially were observed for the weak fluorescence of vascular gels under 488 µm excitation. Vascular gels were stained with ruthenium red (van der Molen et al 1983) to determine pectin content. Freehand sections were stained 1 min using a saturated water solution of ruthenium red, rinsed in distilled water and immediately observed with a light microscope. Pectin stained light pink to red.
Determination of hyphal nuclear complement.— –
Freehand sections of colonized plant tissue were stained with acridine orange following the methods of Sandor et al (2000) to visualize the nuclei. Sections were covered 5 min with 400 µM acridine orange in distilled water, followed by two rinses in distilled water. Samples were observed on a Zeiss Standard epifluorescence microscope using a 488 µm excitation filter.
Treatment of wheat residue.— – Wheat plants (cultivar Norm), grown under field conditions in Ramsey County, Minnesota, were tagged for collection when symptoms were visible. Tagged samples then were removed from the field at grain harvest. Each sample was collected without root material or heads and consisted of a single wheat stem with leaves. Roots were cut away at the soil line and heads were cut away at the top of the peduncle directly below the lowest spikelet of the head. To stimulate perithecium development under field conditions, samples were placed in vinyl mesh bags (1 mm mesh, 43 x 20 cm), two samples to a bag, and returned to the soil surface in Ingham County, Michigan. Two samples were retained for immediate processing.
Microscopy.— – Sections from greenhouse-inoculated plants were observed using either a Zeiss Standard epifluorescence microscope or a Zeiss Pascal 5 laser scanning confocal microscope (LSCM) with a 488 µm krypton laser ( Jena, Germany). For both microscopes, a 488 µm excitation filter was used. For the Zeiss standard microscope, a long pass 520 µm barrier filter allowed for the observation of host autofluorescence and the GFP simultaneously. Images obtained with the Zeiss Pascal 5 were collected in two channels (a long pass 560 µm barrier filter and a band pass barrier filter with a range of 505–530 µm) and were reconstructed using Laser Scanning Microscope LSM 5 Pascal software, version 3.0 SP3. Images from the Zeiss Standard microscope were collected using a Nikon Coolpix 995 (Tokyo, Japan). All images were transferred to Adobe Photoshop 6.0.
The surfaces of field-inoculated wheat stems were inspected for perithecia and collected as perithecia formed. All samples were collected within a period of 3 mo and were processed immediately as follows. Samples (internode, leaf or node pieces, 0.5–1 cm in length) were removed from each stem, with a minimum of three node samples, eight internode samples, four sheath samples and three leaf blade samples per stem. The samples were placed in FAA (3.5% formaldehyde, 5% glacial acetic acid and 47.5% ethanol in water) and vacuum infiltrated. After a 24 h fixation, samples were placed in a solution of glycerol and ethanol (1:1) for an additional 24 h to soften tissues for sectioning. Samples were dehydrated through a tertbutanol series (O’Brien and McCully 1981), embedded in Tissue Prep paraffin wax (Fisher Scientific, Pittsburg, Pennsylvania) and stored at 4 C until sectioned. Embedded samples were sectioned to a thickness of 15 µm using a rotary microtome. Microscopic inspection of serial sections was conducted using a Zeiss Standard microscope (model: GFL 654-633) with phase-contrast optics.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The GFP marker, identifying the ZTE-2a strain, was detected in hyphae descending from the infected head and in the infection front. Wheat heads inoculated with PH-1 (positive control) developed symptoms equivalent to those inoculated by ZTE-2a. Wheat heads inoculated with distilled water (negative control) exhibited no disease symptoms in the head or culm.
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). In the presence of occlusions, the lumen of the vessels stained pink with ruthenium red (FIG. 4), and the walls of the vessels, phloem and cells stained pink, indicating the production and extrusion of pectin-containing compounds (Beckman and Roberts 1995).
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) and pith cavity as hyphae descended. This pattern was maintained at the infection front, making the vessels and pith cavity the two major means of mycelial progression down the stem. At 14–16 dai, established hyphae within the vessels and pith cavity began to branch and grow radially. Radial colonization was initiated with the movement of hyphae into intercellular spaces between the xylem and fibers of the vascular bundles and through the parenchyma near the pith cavity (FIG. 6). At 15–17 dai hyphae penetrated xylem cells in direct contact with vessels and phloem, initiating intracellular growth. This intracellular growth also extended to parenchyma cells in contact with the vascular bundles. Hyphae then grew from cell to cell through pits (FIG. 7) and by direct penetration of adjacent cells (as described by Wanyoike et al [2002]). Colonization continued outward and the chlorenchyma, just below the stem surface, was reached at 16–18 dai. Hyphae filled sub-stomatal cavities of exposed culms (not covered by leaf sheaths) but did not grow through stomates. The heavily lignified fibers underlying the epidermal cells and the cutinized epidermis were rarely colonized. Two distinct symptoms were observed on culm and sheath surfaces as stems were colonized. Chlorosis first was observed near the rachis at 14–16 dai and was associated directly with the initiation of horizontal colonization. At 16–18 dai, brown streaks appeared on stem surfaces, simultaneously with the colonization of the chlorenchyma. This pattern of colonization continued down the stems until the uppermost node was reached.
Node colonization was initiated by hyphae moving down the pith cavity and was characterized by inter-cellular growth between parenchyma cells comprising the central part of the node at the leaf base (FIG. 1). Hyphae grew between the parenchyma cells into the vascular traces at the joint of leaf. The xylem and phloem were penetrated and colonized and from there hyphae moved into the culm (FIG. 8) and pith below the node. The colonization of subsequent node and internode regions followed a similar pattern as described above.
The colonization of leaf sheaths was initiated as hyphae protruded through culm stomata and filled the space between culm and sheath. Hyphae within this space colonized downward similarly to hyphae in the pith cavity. Hyphae penetrated the adaxial surface of the leaf sheath and began intercellular growth. Colonization proceeded through the sheath mesophyll, both inter- and intracellularly. Hyphae continued to grow toward the abaxial surface, colonizing vascular bundles and filling substomatal cavities. Vessels within the vascular bundles of the leaf sheath were penetrated by hyphae, which did not colonize further. Hyphae that reached stomatal cavities formed perithecial initials below stomates. Some hyphae emerged from stomates on the abaxial surface of the leaf sheath and grew across the leaf surface.
Anatomy of colonizing hyphae.— –
Hyphae colonizing wheat stems had three distinct morphologies: thin and uninucleate, wide and dikaryotic and curled into perithecium initials. Young hyphae were thin, regularly septate and uninucleate. These hyphae occurred at the infection front in vessels and in the pith cavity. Growth by uninucleate hyphae was both intra-cellular and intercellular throughout stem tissues and the most frequently observed hyphal form. As uninucleate hyphae became established within the vessels, pith cavity and chlorenchyma, they developed into dikaryotic hyphae composed of short, wider cells (FIGS. 9, 10). We use the term dikaryotic to describe cells with paired nuclei. Because the fungus is homothallic, the term as used here does not imply genetic differences between the nuclei. Staining with acridine orange confirmed the nuclear state of the hyphae. Hyphae were not considered dikaryotic unless all of the cells were observed to contain paired nuclei and a minimum of four successive cells could be distinguished. Established dikaryotic hyphae within the vascular bundles and pith cavity branched to form uninucleate hyphae, which initiated radial colonization. Dikaryotic hyphae growing within the chlorenchyma and the substomatal cavities gave rise to perithecium initials (FIG. 11) that eventually filled the substomatal cavities.
Development of perithecia in field-grown plants.— – Whereas strain ZTE-2a readily colonized stems, it did not produce perithecia. Therefore, field-grown wheat stems were used to investigate the final stages of perithecium development in planta. Colonization patterns within field-inoculated stems were assessed before and after perithecium development. While the process of colonization was not examined in field-inoculated samples, the pattern of colonization in mature plants confirmed observations for greenhouse-inoculated plants. Thus intracellular and inter-cellular colonization by uninucleate hyphae was observed throughout stem tissues and dikaryotic hyphae developed in the pith cavity, vascular bundles and chlorenchymatous tissue. Infection fronts were not present within field-inoculated wheat stems, as the stems were fully colonized at collection.
Perithecia developed on nodes and internodes of all wheat stems recovered after field treatment. Internode epidermis was composed of stomatal guard cells, silica cells and cork cells dispersed in a field of elongated epidermal cells. Node epidermis was composed of silica and cork cells similarly distributed among elongated epidermal cells. On culms and leaf sheaths, perithecia emerged only above stomatal openings (FIGS. 12, 14, 15). Perithecium emergence was limited to stomata and silica cells in the node regions (FIGS. 13, 17).
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Perithecium development on sheathes was associated directly with colonization and development of hyphae from underlying internode tissue (FIG. 16). Where sheath tissue covered culm stomata, perithecium initials formed in the substomatal cavities of the culm, but instead of continuing to develop, hyphae emerged through the stomatal pores to the abaxial sheath surface. Hyphae then grew through the chlorenchyma cells of the sheath and formed new initials in the substomatal cavities of the adaxial sheath surface. Perithecium development in internode stem tissue occurred where stomates were exposed and chlorenchyma cells were colonized.
Perithecium development on node tissue was dense in comparison to development on internode tissue. Perithecia formed from epidermal cells adjacent to silica cells in nodes, but hyphae did not colonize silica cells (FIG. 16). Perithecia were most numerous on the ridges of the node, where silica cells were dense.
Early development of perithecia in nodal regions was initiated by the growth of wide hyphae within the epidermal and parenchyma cells. However the nodes did not have stomates except at their boundaries. In the absence of stomates, perithecium initials formed within epidermal cells and were much smaller relative to those formed in substomatal cavities of the internodal region. Perithecia erupted from the epidermal cells or infrequently, formed from within a stroma that developed on the node surface, but always in association with a silica cell. Despite the presence of scattered silica cells among the stomates on the internode surface, perithecia were not observed emerging from epidermal cells adjacent to silica cells of the internode.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In other ascomycetous fungi, dikaryotic hyphae have been associated only with sexual development. To our knowledge this is the first report of progression from uninucleate hyphae to dikaryotic hyphae and back to uninucleate hyphae. Trail and Common (2000) observed dikaryotic hyphae near the surface of culture plates in regions where perithecia were forming. In the findings of the present study and that of Trail and Common (2000), dikaryotic hyphae were wider than uninucleate hyphae, a characteristic that could imply storage in preparation for survival. Trail and Common (2000) found that wide hyphae contained many refractive drops that stained positive for lipids.
The formation of perithecia was associated with specific host cells: stomatal openings and silica cells. Light has been shown to be required for the formation of perithecia (Tschanz et al 1976) and could be a factor that induces the maturation of perithecia through stomatal openings and light-transmitting silica cells. In support of this hypothesis, mature perithecia developed in stomatal openings only when light was present. Thus, when the sheath covered the culm, mature perithecia developed only on the sheath surface (FIG. 16). However, perithecium initials were formed below stomates and silica cells regardless of the presence of light, indicating that the first signal for perithecium development might be a result of hostpathogen interaction and a subsequent signal (possibly light related) is required for further development. Because initials develop and go dormant frequently, the presence of two distinct signals is expected. The lack of perithecium development on silica cells of the internodes might be explained in part by the presence of fiber cells directly beneath the silica cells in this region (unpublished observation). The fungus did not readily colonize fiber cells. In the areas immediately surrounding the stomates, silica cells also were present. Here too perithecium initials were not associated with silica cells, a fact that remains unexplained. Further studies of the regulation of sexual development obviously are needed. Functional genomics studies of plant and fungal interactions are being used to elucidate the basis of this phenomenon.
Within wheat culms, colonizing hyphae moved through xylem vessels before colonizing other tissues. Tu (1953), Ribichich et al (2000) and Wanyoike et al (2002) observed that the vascular bundles leading from the spikelet to the rachis and the bundles of the rachis were well colonized. They hypothesized that the vascular system was important to the colonization process of the head, a process we have now confirmed in the vegetative tissues as well. The phloem and chlorenchyma of the culm were especially damaged as a result of colonization by G. zeae. Both tissues were discolored and degenerated after fungal infection. Pugh et al (1933) and Tu (1953) reported similar damage in the same tissues of the rachis and glumes within wheat heads. Pugh et al (1933) observed that as mycelia amassed beneath epidermal tissues, sporodochia erupted through the epidermis. This was not observed in this study, although in field samples, sporodochia erupted from the stomata in samples examined just after har vest (data not shown).
In this study, 25% of all plants inoculated did not develop symptoms that extended into the culm. The inability of the fungus to colonize culms in these plants is due likely to an unstable Type II (resistance to spread of infection) resistance mechanism within the wheat cultivar Norm. The occlusions in the xylem vessels stained red with ruthenium red indicating they are most likely pectic gels similar to occlusions reported for other vascular diseases (van der Molen et al 1983, Bishop and Cooper 1984). Ribichich et al (2000) reported that vascular occlusions were present in the highly resistant wheat cultivar Sumai-3 after inoculation but were not present in susceptible cultivars of wheat. Vascular occlusions are an important component of resistance for many plants that are hosts to vascular pathogens (Beckman and Roberts 1995) and might also be an important component of resistance to FHB for wheat.
We have shown that colonization of wheat vegetation before grain harvest in the field is an important step in perithecium development. Vegetation might become colonized by means of stem-base infections and head infections, letting the head blight pathogen establish itself before saprophytic invasion by other organisms. Strategies to control or eliminate inoculum in the field should focus on slowing or reducing the colonization of wheat vegetation and reducing sporulating structures on debris surfaces. An obvious target for the reduction of vegetative colonization is Type II resistance mechanisms. Reducing sporulation on debris will require a further understanding of the factors that initiate sporulation. An understanding of these processes will aid in measures to reduce potential inoculum production and survival by this fungal plant pathogen.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: trail{at}pilot.msu.edu
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LITERATURE CITED |
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Beckman CH, Roberts EM. 1995. On the nature and genetic basis for resistance and tolerance to fungal wilt diseases of plants. In: Callow JA, ed. Advances in botanical research incorporating advances in plant pathology. St Paul, Minnesota: APS Press.
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