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Mycologia, 94(3), 2002, pp. 505-514.
© 2002 by The Mycological Society of America

The biological cycle of Sporisorium reilianum f.sp. zeae: an overview using microscopy


Carole Martinez
Christophe Roux 1

     Unité Mixte de Recherche 5546, Equipe de Mycologie Végétale, Université Paul Sabatier/CNRS, Chemin de Borde-Rouge, Pôle de Biotechnologie Végétale, BP 17, 31326 Castanet Tolosan, France

Alain Jauneau

     Institut Fédératif de Recherche, I.F.R. 40, CNRS, Pôle de Biotechnologie Végétale, 31326 Castanet Tolosan, France

Robert Dargent

     Unité Mixte de Recherche 5546, Equipe de Mycologie Végétale, Université Paul Sabatier/CNRS, Chemin de Borde-Rouge, Pôle de Biotechnologie Végétale, BP 17, 31326 Castanet Tolosan, France

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

Sporisorium reilianum f.sp. zeae is the causal agent of maize head smut. Using microscopy, we describe the development of the fungus during its saprophytic and parasitic phase. When compatible, the yeast forms fused to produce dicaryotic hyphae. These hyphae were infectious and penetrated the maize in the root. Surprisingly, the formation of conjugation tubes was rarely observed in vitro. In contrast, extensive development of long hyphae was observed from the haploid form of the yeast, these hyphae being able to fuse when arising from compatible strains. In planta, the fungus acted as a biotrophic endophyte until sporogenesis, which occurred in the floral meristem of the maize. The symptoms of the infection were reduced. Penetration in the root was never accompanied by drastic damage of the host cell and we did not observe thickening or apposition of plant material to reinforce the wall structure. Moreover, the fungus was embedded in an amorphous matrix and thus appeared isolated from the host cell. In the floral meristem, radical changes were observed, the host cell was totally invaded by the fungus in the course of sporogenesis. The deposits observed on the fungal wall are likely related to the echinulation of the teliospores.

Key words: head smut, maize, Ustilaginaceae


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Sporisorium reilianum f.sp. zeae (Kühn) Langdon & Fullerton is a fungus (Basidiomycota, Ustilaginaceae) that causes head smut of corn (Zea mays L.). Sporisorium reilianum can infect maize and sorghum plants (Al-Sohaily et al 1963Citation ). This disease is present in most areas where maize is frequently grown. Before the appearance of smutted ears, chlorotic flecks on leaf and anthocyan accumulation on stem can be observed (Matyac and Kommedhal 1985Citation ). These symptoms are discrete and often difficult to detect, especially in the field, as chlorotic flecks are usually reversible (Roux pers obs). Additional symptoms like stunting and phyllody are observable for very susceptible inbred maize lines (Stromberg et al 1984Citation ). Crop losses resulting from the infection of maize are due to the formation of a sorus in place of the ear and sometimes the tassel. It has been reported that up to 80% of maize plants can be smutted in an infected field (Frederiksen 1977Citation ). In spite of the agronomic extent of this disease, the description of the life cycle of S. reilianum f.sp. zeae is incomplete.

Teliospores present in sori of smutted corn are disseminated by wind. When temperature and soil moisture are optimal (Baier and Kruger 1962Citation , Téféri et al 1989Citation ), the teliospores germinate in the soil as a four-celled basidium (= promycelium) that presents its lowermost septum above the teliospore cell wall as described for other species of Sporisorium (Ingold 1994Citation ). Each basidium germinates into a large number of haploid basidiospores, which bud like yeast to form sporidia. Compatible haploid sporidia can fuse to give infectious dicaryotic hyphae. The morphological events of the fusion between two compatible haploid yeasts have been widely described in Ustilago maydis (Snetselaar 1993Citation ) and on Microbotryum violaceum (= U. violacea) (Day and Jones 1968Citation ), but not in S. reilianum f.sp. zeae. The genetics of the mating system of Ustilaginaceae is also well documented (Banuett and Herkowitz 1988Citation , Bakkeren and Kronstad 1993Citation , Kahmann et al 1995Citation ). It is known that two genetic loci (named a and b) control the fusion of sporidia on S. reilianum f.sp. zeae (Hanna 1929Citation , Mankin 1953Citation ), although the number of b alleles has not been characterized as it has for U. maydis (Holton et al 1968Citation ).

Sporisorium reilianum f.sp. zeae infects maize only via roots when for most of the other Ustilaginaceae the infection occurs either via root or aerial parts. For instance, U. maydis can develop an appressorium at the surface of young leaves and stigmatas (Snetselaar and Mims 1992, 1993Citation ), whereas on aged leaves, penetration seemed to occur via stomata and wounds (Mills and Kotzé 1981Citation ). In contrast, S. reilianum f.sp. zeae locally dissolved the epidermal cell wall to penetrate the maize root and never developed an appressorium at the root surface (Martinez et al 2000Citation ).

In planta, little is known and most of the information concerns the status of the fungus in the smutted inflorescence of maize and sorghum. For instance in maize, S. reilianum f.sp. zeae forms sporogenous hyphae, partitioning hyphae between spore balls and nonsporogenous intercellular hyphae (Fullerton 1970Citation , Langdon and Fullerton 1975Citation ). Under electron microscopy, a gelatinous matrix was observed around the sporogenous hyphae of U. maydis (Fisher and Holton 1957Citation ) and S. sorghi (Mims and Snetselaar 1991Citation ). In the vegetative shoot apex, the hyphae of S. reilianum f.sp. zeae were embedded in a polysaccharidic matrix (Martinez et al 1999Citation ).

The description of the life cycle of S. reilianum f.sp. zeae is mainly limited to the early steps of sporogenesis. There are few data on the ultrastructure of the fungus in vegetative parts of maize and no information are available on the behavior of the fungus during the pre-infectious stage. The aim of this paper is to present an overview of the life cycle of S. reilianum f.sp. zeae investigated using microbiological and microscopic techniques.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Biological material and culture – Teliospores of Sporisorium reilianum f.sp. zeae were collected in a maize field at Saint-Sauveur (Haute-Garonne, France) and stored in tubes containing silica gel (Sigma, USA). They were rinsed twice for 10 min in sterile distilled water, treated for 12 min in 2% (w/v) chloramine T (Sigma, USA) and thereafter washed in sterile distilled water. Germination of teliospores was performed on Petri dishes containing potato dextrose agar (PDA, Difco Laboratories, USA). Compatible haploid basidiospores were collected from one teliospore by micromanipulation (de Fontbrune, France). Each strain of basidiospore was maintained in potato dextrose broth (PDB, Difco Laboratories, USA), at 24 C under shaking. For mating, compatible haploid strains were mixed during 48 h in PDB at 24 C under shaking. A drop of this culture was then deposited on minimal medium [10 g glucose, 3 g KNO3, 1 mg thiamin, 0.5 mg riboflavin, 2 mg calcium pentothenate, 2 mg nicotinic acid, 10 mg inositol and 62.4 mL Holiday's salt solution (Holliday 1974Citation ) at pH 7.0] solidified with 0.5% (w/v) gellan gum (Phytagel, Sigma, USA). Maize seeds from a susceptible corn variety (Z. mays, variety DK 300, R.A.G.T., France) were sterilized with an aqueous solution of chloramine T (Sigma, USA) (2% w/v) for 15 min, and then washed with sterile distilled water. To test the efficiency of this treatment, seeds were germinated on PDA for 3 d at 24 C. Seedlings free of microbial-contamination were transferred to sterilized peat (1 h at 120 C) and then cultivated in a greenhouse at 24 ± 5 C. At the time of the transfer in peat, the maize seedlings were inoculated by adding 0.5 mL of a suspension of sterile teliospores (106 teliospores mL-1, teliospores being counted under the microscope using a Thoma cell). For observation of penetration, assays were performed on solid medium in Magenta boxes (Martinez et al 2000Citation ).

Light and electron microscopy – Samples were mounted on a glass slide and were observed using an inverted microscope (Leitz DMIRBE, Leica, Germany). Images were acquired using a CCD camera (Color Coolview, Photonic Science, UK) and treated by image processing (Image Pro Plus, Media Cybernetics Maryland, USA). Some fungal cells were fixed in 3% glutaraldehyde in 0.05 M phosphate buffer saline (PBS) pH 7.4 for 20 min and treated in a drop of Triton x100 for 15 min. They were placed in glycerol solution, rinsed and finally stained with 1/20 wheat germ agglutinin-fluorescein isothiocyanate (WGA-FITC, Sigma, USA) in PBS for 30 min. Finally, they were rinsed and mounted in the same buffer. For scanning electron microscopy, samples prepared according to Martinez et al (2000)Citation were sputter-coated with gold palladium using a Jeol JFC 1100 and examined with a Hitachi C450 scanning electron microscope at 15 kV. Photographs were taken using an Illford 125 ISO film. For transmission electron microscopy, small pieces were embedded either in LR White or Spurr'epoxy and Epon resin as previously reported (Martinez et al 1999Citation ). Semi-thin (1 µm) and ultrathin sections (50–60 nm in thickness) were cut with a diamond knife using a Reichert Ultracut E microtome (Leica, Germany) and collected on gold grids. Semi-thin sections were stained using toluidine blue. Ultrathin sections were stained either by PATAg (periodic acid, thiocarbohydrazide, silver proteinate) treatments for total polysaccharide visualization, or uranyl acetate (10 min) and lead citrate (5 min). They were observed using a Philips 301 transmission electron microscope at 80 kV (Philips, The Nederlands).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
In vitro growth – Brown teliospores were collected from maize head smut (Fig. 1 ). The teliospores germinated into four-celled basidia producing lateral basidiospores. They were isolated using a micropipette (Fig. 2 ), and then cultivated either in liquid or solid medium. In liquid medium (Fig. 3 ), the haploid basidiospores reproduced by budding. The budding scar, showing the point of separation between two yeasts, was heavily stained by means of WGA-FITC probe (Fig. 4 ). Sometimes pseudohyphae resulting from the nonseparation of dividing yeasts were observed (not shown). The formation of conjugation tubes arising from sporidia was observed after 48 h of culture of a mixture of two compatible haploid strains (Fig. 5 ). The fusion of these conjugation tubes led to the formation of hyphae (Fig. 6 ). On solid medium, the haploid strains of the fungus developed long hyphae which were able to fuse (Figs. 7, 8 ). These hyphae were characterized by the presence, at regular intervals, of septa stained by WGA-FITC (Fig. 9 ). The septa delimited empty cells except at the growing tip (Figs. 7, 8, 10 ).



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  		 FIGS. 1–10. Light (LM), and transmission electron micrographs (TEM) of S. reilianum f.sp. zeae during its saprophytic phase. 1. Smutted ears (arrows) of maize. 2. Four-celled basidium (arrow) from a brown teliospore (T) producing lateral basidiospores (arrowheads). Each basidiospore was collected using a micropipette (MI). Bar = 14 µm. 3. Budding yeasts in liquid medium. Bar = 8 µm. 4. WGA-FITC labelling shows the point of separation between two budding yeasts. Bar = 6 µm. 5. Conjugation tubes are visible (arrows). Bar = 12 µm. 6. Their fusion, when haploid strains were compatible, gives rise to a hypha (arrow). Bar = 10 µm. 7. On solid medium, development of long hyphae (arrows) from haploid strains. The hyphae were composed of empty cells except for the apical cell at the growing tip (arrowheads). Bar = 20 µm. 8. The fusion between two haploid hyphae is possible and leads to the formation of another hyphae (arrow). Bar = 14 µm. 9. Visualization of the septa at regular intervals along the hyphae by means of WGA-FITC labelling. Bar = 8 µm. 10. At the TEM level, the growing tip exhibits an apical cell containing numerous organelles. Note that the proximal cells (arrows) are empty and constricted. Bar = 1.5 µm

 
Root penetration – Three weeks after inoculation, plantlets cultivated in Magenta boxes did not present any symptoms (Fig. 11 ). Nevertheless, the root surface was largely colonized by the fungus as shown by either optical microscopy (Fig. 12 ) or scanning electron microscopy (SEM) (Fig. 13 ). The same observations were made with plantlets cultivated in peat (not shown). With electron microscopy, short pieces of broken fimbrial-like structures were observed around the fungus cells (Fig. 14 ), some of them being inserted into host cell walls (Fig. 15 ). Fungal cells appeared against or tightly attached to the root epidermal wall (Fig. 14 ). At the SEM level, it was observed that hyphae passed through the epidermal cell wall (Fig. 16 ). Further observations were made with maize cultivated and inoculated in peat. In roots, the fungus was mainly observed in the cellular compartment (Fig. 17 ). Hyphal septation was visible and the fungal cell was surrounded by fibrillar PATAg-stained polysaccharides. In some cases, the root cells were totally invaded by the fungus (Fig. 18 ). In both pictures, the host cell walls appeared unaltered even when the fungus was observed in the tricellular junction.



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  		 FIGS. 11–16. LM, TEM and scanning electron micrographs (SEM) obtained during the infection of the maize root. 11. Maize infected by S. reilianum f.sp. zeae and cultivated in Magenta box exhibited no symptoms. 12. Transverse section of infected root stained by toluidine blue. The root is surrounded by a sheath composed of numerous fungal cells (arrowheads). C = cortex, V = vessel. Bar = 60 µm. 13. The fungal sheath (S) as seen by SEM. Long hyphae were tightly bound to the root surface (R). Bar = 100 µm. 14. Fimbrial structures (arrowheads) are observed by TEM around the fungus cells (FC) and in contact with the host cell wall (CW). Bar = 1.5 µm. 15. At higher magnification, the tripartite structure of the fimbriae (arrowheads) and their insertion in the host cell wall (CW). Bar = 100 nm. 16. Hyphae (H) passing through the epidermis (E). At the point of contact, only a small pad (arrow) is visible. Bar = 1.5 µm

 


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  		 FIGS. 17–22. Colonization of the maize plant. The transverse sections were PATAg- stained and observed by TEM. 17. The fungus in the root cell is surrounded by a fibrillar matrix (arrows). Note the septation (arrowhead) of the fungal cell. Bar = 1.5 µm. 18. Some root cells are totally invaded by the fungus. Note the presence of the fungal cell in the tricellular junction (arrowhead). Bar = 2 µm. 19. In the stem, the fungus cells are surrounded by a matrix (arrows) that is more dense than in the root cells. Some hyphae are collapsed (arrowheads). Bar = 1.5 µm. 20. Chlorotic flecks (arrows) on leaves. 21. In the chlorotic flecks, the hyphae (arrowheads) were always collapsed and surrounded by a matrix (arrows), the host cell was damaged and chloroplasts (CH) were disrupted. Bar = 0.5 µm. 22. In the vicinity of the chlorotic flecks, the plant cells were unaltered with numerous chloroplasts (CH). Bar = 1.5 µm. CW = host cell wall, FC = fungal cell, N = nucleus.

 
In planta growth – In the stem, the fungus was also observed in the cellular compartment as in the root cells. However, in the part of the stem showing anthocyan accumulation, some fungus cells were collapsed (Fig. 19 ). The external matrix surrounding the fungal cell was more dense and thicker than that observed in the root cells. The main symptom in the vegetative part of maize was the development of chlorotic flecks on leaves (Fig. 20 ). In the middle of these flecks the fungus was always collapsed. The matrix surrounding the fungal cells seems to extend to the host cell wall (Fig. 21 ). The organelles of the chlorotic plant cell host were altered and only some chloroplastic structures were recognizable. However, in the vicinity of the chlorotic spots, the plant cells were unaltered with numerous chloroplasts around the nucleus (Fig. 22 ). In the vegetative apex, the fungus was observed either in intercellular spaces or in the host cells. All the fungal cells were surrounded by a sheath that was encapsulated by a plasmalemmic membrane (Fig. 23 ). The host cells were never altered by the presence of the fungus. Sometimes, the hyphae were collapsed (not shown).



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  		 FIGS. 23–27. Infection of the apical meristem and sporulation. PATAg-stained transverse sections. 23. In the vegetative shoot apex, the fungal cell (FC) embedded in its matrix is surrounded by a membrane (arrow). The host cells were unaltered. Bar = 0.8 µm. 24–27. Status of the fungus in the floral shoot apex. 24. A fungal cell (FC) passing through the host cell wall (arrows) without disruption of the plasmalemma (arrowheads). The host cell was not altered by the presence of the fungus. Bar = 2 µm. 25. In other cases, either the fungal cells were collapsed (arrows) and the host cell unaltered, or both cells were distroyed (arrowheads). Bar = 3 µm. 26. Finally, some host cells were totally invaded by numerous fungal cells (FC). Deposits (arrowheads) were observed on certain fungal cell walls. Bar = 3 µm. 27. Higher magnification of the deposits on the fungal cell wall. Bar = 1 µm. CW = host cell wall, FC = fungal cell; N = nucleus, V = vacuole.

 
Sporogenesis – After the transition of the vegetative apex to the floral meristem of maize, the fungus cells were mostly intracellular. Four types of interaction between the fungus and the host cells were observed: (i) Hyphae and the host cells did not exhibit any alteration (Fig. 24 ); (ii) the fungal cells were collapsed and the host cell unaltered (Fig. 25 ); (iii) both fungal and plant cells were dramatically damaged (Fig. 21 ); (iv) the fungus was unaltered and totally invaded the host cells, which were destroyed (Fig. 26 ). This feature corresponds to the sporogenous step, and the maturation of spores was characterized by the formation of an ornamentation at the surface of the wall (Fig. 27 ).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Like most Ustilaginaceae, the life cycle of S. reilianum f.sp. zeae exhibits two phases, a yeast saprophytic and a mycelium parasitic phase. Transition between the two phases is related to the sexuality of the fungus: (i) yeast-to-mycelium transition arises when compatible haploid strains mate to form infectious dicaryotic hyphae, and (ii) transition from diploid mycelium to haploid yeast occurs via meiosis during teliospore germination. However, some aspects of the biology of S. reilianum f.sp. zeae have to be underlined and will be discussed: (i) the ability to form haploid hyphae, (ii) the relationships between the fungus and its host during its growth from the roots up to the apical meristem, (iii) the transition from biotrophic to necrotrophic behavior of the fungus in the floral meristem.

In vitro haploid hyphae – In Ustilaginaceae, it is usually accepted that hyphae originate from dicaryotic cells resulting from the fusion of compatible haploid strains. Compatible strains have different alleles of the b mating-type gene, the by-products of the two alleles interacting to regulate the growth of dicaryotic cell (Hartmann et al 1996Citation ). However, we observed that haploid strains of S. reilianum f.sp. zeae cultivated on solid medium were able to form numerous hyphae. This result indicates that hyphal growth is not specific to dicaryotic cells and that alternative mechanisms could be involved. The yeast-to-mycelium transition of haploid strains could be favored by environmental factors. Asexual dimorphic switching of Ustilaginaceae in response to physiological parameters has been reported for pH and nutrient starvation (Ruiz-Herrera et al 1995Citation , Martinez-Espinoza et al 1997Citation ) and it has been suggested that the promoting effect of different carbon sources on hyphal growth in S. reilianum f.sp. reilianum could be due to the inability of the fungus to metabolize the nutrients tested (Bhaskaran et al 1991Citation , Bhaskaran and Smith 1993Citation , Lichter and Mills 1997Citation ). Plant extracts were also known to promote the change from yeast to hyphal form in Ustilago violacea, Ustilago maydis, and Sporisorium reilianum (Day et al 1981Citation , Bhaskaran et al 1991Citation , Ruiz-Herrera et al 1995Citation , Bhaskaran and Smith 1995Citation ). Whatever the factors involved in hyphal growth, the biological significance of the filamentization of haploid strains is unclear. Haploid strains cannot infect maize (data not shown). This indicates that although different dimorphism regulation pathways could be involved, induction of parasitism is only regulated by the products of the b mating-type genes like for other Ustilaginaceae (Gillissen et al 1992Citation , Yee and Kronstad 1998Citation ). This underlines that hyphal growth and parasitism are two physiological responses whose regulatory pathways could be partly deconnected. We can speculate that development of haploid hyphae in the rhizosphere allows S. reilianum f.sp. zeae to explore the environment, increasing the opportunities to mate, and to meet a maize root, and thus enhance its infection efficiency.

Biotrophic growth – In our assays, the infected plants were symptomless. Even at the first step of infection (i.e. root cell penetration) there is no apparent reaction of the plant cells (Martinez et al 2000Citation ). Cytolocalization of S. reilianum f.sp. zeae demonstrated that hyphae were mostly intracellular. Around the intracellular hyphae we always observed an amorphous matrix. A similar matrix has been observed in many other fungal-plant interactions (Hardham and Mitchell 1998Citation ). Hutchinson et al (1996)Citation demonstrated that plant compounds were present in the interfacial material between the hyphae of Colletotrichum lindemuthianum and bean cells. Whatever the exact origin and composition of the matrix, the fungus is bordered by the matrix and thus isolated from the host cells. Altogether, our results suggest that the fungus acts like a biotrophic endophyte from the root up to the vegetative meristem of maize (Martinez et al 1999Citation ). This idea is in accordance with a high degree of compatibility between the smut fungi and their hosts (Luttrel 1987Citation ). This is particularly true for S. reilianum f.sp. zeae which causes minimal symptoms on the leaves and stems.

Sporogenesis and Necrotophic growth – The sporogenesis of S. reilianum has been described in sorghum (Wilson and Frederiksen 1970Citation ) and in maize (Langdon and Fullerton 1978Citation , Matyac 1985Citation ). These authors described different types of hyphae in the mature sorus: peridial, reproductive and vegetative hyphae (Clinton 1897Citation , Wilson and Frederiksen 1970Citation ). Langdon and Fullerton (1975)Citation proposed that in maize vegetative hyphae be separated into partitioning hyphae (between spore balls) and nonsporogenous intercellular hyphae. In young sori, we observed only one type of hypha similar to those observed in maize vegetative tissues. Further specialization of vegetative hyphae could occur to form peridial hyphae around the sorus. Some meristematic host cells were totally invaded by the fungus. This invasion is likely related to the induction of sporogenesis since we observed echinulation at the fungus cell wall surface. Echinulation corresponds to melanization of teliospores during maturation, forming spines at the surface of the teliospores as previously described on S. sorghi (Mims and Snetselaar 1991Citation ). The most striking feature is that sporogenesis induction in the fungus is concomitant with floral initiation of the maize. When the fungus becomes necrotrophic, floral tissue decline is induced. Some changes in the host tissues during floral initiation are likely perceived as a signal by the fungus to induce sporogenesis. So, the floral dependence of S. reilianum f.sp. zeae sporogenesis might be used to detect early signals of floral induction, which has been successfully performed for other tissue-specific fungi (Scutt et al 1997Citation ).

To conclude, it must be pointed out that the most striking feature of the behavior of S. reilianum f.sp. zeae is its ability to decrypt the physiological events occurring in the development of maize.


   ACKNOWLEDGMENTS
 
In memory of our esteemed colleague, Pr. Robert Dargent.


   FOOTNOTES
 
1 Corresponding author, roux{at}smcv.ups-tlse.fr Back

Accepted for publication October 4, 2001.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
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