Cytology and ultrastructure of interactions between Ustilago esculenta and Zizania latifolia

Abstract

Ustilago esculenta is a biotrophic smut fungus that parasitizes Zizania latifolia, an edible aquatic vegetable of the southern China region. Infection results in swelling of the upper parts of the Z. latifolia culm which are called jiaobai and have a unique flavor and delicacy and are popular among Chinese. The infection process of Z. latifolia by U. esculenta was investigated with light and electron microscopy. Distribution of hyphae was uneven in plants; hyphae were mainly present in the swollen upper parts (jiaobai), the nodal regions of mature culms and old rhizomes and buds or shoots. Hyphae were rare in the internodes of mature culms and were fewer in the internodes of old rhizomes. All new buds produced on the nodes of culms and rhizomes were infected by hyphae in November before and in March after overwintering. The hyphae grew into the buds from the parent nodes via intervascular tissues only or via parenchyma tissues and vascular bundles. Hyphae extended within and between the host cells and frequently formed hyphal aggregations or clusters, not only in the mature tissues but also in developing tissues. The typical interface between the fungal hyphal wall and invaginated host plasma membrane comprised a sheath. The sheath surrounding a hyphae comprised an outer electron-opaque matrix and an inner electron-dense layer. The electron-opaque matrix layers were thicker in jiaobai tissues, ranging from 0.28 to 0.85 μm. The electron-dense hyphal coatings were more conspicuous in the young buds or shoots and mature culms than in the jiaobai. The intercellular hyphae caused large cavity formation between the cells or rupture of host cell walls, for gaining entry into host cells. The broken host cell wall fused with the electron-opaque matrix of the hyphal sheath as an interactive interface. The teliospore wall and wall ornamentation development was the same in postmature jiaobai tissues with sporadic sori and in the huijiao (jiaobai tissues containing the massive sori), but a sheath enveloping the teliospore was more transparent in the process of teliospore development in the jiaobai than in the huijiao.