Abstract
The smut fungus Ustilago esculenta infects Zizania latifolia and induces stem expansion to form a unique vegetable named Jiaobai. Although previous studies have demonstrated that hormonal control is essential for triggering stem swelling, the role of hormones synthesized by Z. latifolia and U. esculenta and the underlying molecular mechanism are not yet clear. To study the mechanism that triggers swollen stem formation, we analyzed the gene expression pattern of both interacting organisms during the initial trigger of culm gall formation, at which time the infective hyphae also propagated extensively and penetrated host stem cells. Transcriptional analysis indicated that abundant genes involving fungal pathogenicity and plant resistance were reprogrammed to maintain the subtle balance between the parasite and host. In addition, the expression of genes involved in auxin biosynthesis of U. esculenta obviously decreased during stem swelling, while a large number of genes related to the synthesis, metabolism and signal transduction of hormones of the host plant were stimulated and showed specific expression patterns, particularly, the expression of ZlYUCCA9 (a flavin monooxygenase, the key enzyme in indole-3-acetic acid (IAA) biosynthesis pathway) increased significantly. Simultaneously, the content of IAA increased significantly, while the contents of cytokinin and gibberellin showed the opposite trend. We speculated that auxin produced by the host plant, rather than the fungus, triggers stem swelling. Furthermore, from the differently expressed genes, two candidate Cys2-His2 (C2H2) zinc finger proteins, GME3058_g and GME5963_g, were identified from U. esculenta, which may conduct fungus growth and infection at the initial stage of stem-gall formation.
Highlights
Zizania latifolia Turcz. is a perennial aquatic plant that is an ancient cereal crop and has been cultivated for more than 2000 years in China [1]
A small number of round or irregular spores were sporadically distributed in the nonswollen tissue, while a large number of hyphae were dense and vigorous, showed a network and winding pattern, and tended to extend to the interior of the host tissue at 0 d of stem-gall formation (Figure 2B)
Previous studies have characterized some genes related to stem enlargement in Z. latifolia and U. esculenta separately [10,37,38], but the analyses were not sufficiently systematic or comprehensive
Summary
Zizania latifolia Turcz. is a perennial aquatic plant that is an ancient cereal crop and has been cultivated for more than 2000 years in China [1]. U. esculenta is a number of smut fungi belonging to the basidiomycetes Smut fungi, such as U. maydis, Sporisorium reilianum, U. hordei, Urocystis tritici, and Thecaphora solani, consistently cause devastating effects on the host plant, preventing crop growth and causing huge economic losses; smut disease is sometimes the reason for famine in any particular area or place [4,5]. While during the long process of artificial selection and coevolution, U. esculenta and Z. latifolia reached a clever balance between plant’s disease resistance and fungal infection [3,6], the infected stem was no longer a common disease tumor (full of black powder) but formed an edible, white swollen culm gall, which was found to be delicious and nutritious, was deeply loved by the people and was called “Jiaobai” in China [6,7]. Jiaobai cultivation has become a pillar industry in some areas of the Zhejiang and Jiangsu provinces and other regions in China, and has high economic value [1,8]
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