Ustilago maydis Infection Strongly Alters Organic Nitrogen Allocation in Maize and Stimulates Productivity of Systemic Source Leaves

Ustilago maydis Infection Strongly Alters Organic Nitrogen Allocation in Maize and Stimulates Productivity of Systemic Source Leaves
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DOI:
10.1104/pp.109.147702
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发表时间:
2010-01-01
期刊:
影响因子:
7.4
通讯作者:
Voll, Lars M.
Voll, Lars M.
中科院分区:
生物学1区
文献类型:
--
作者:
Horst, Robin J.;Doehlemann, Gunther;Voll, Lars M.

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担子菌玉米黑粉菌 (Ustilago maydis) 是玉米黑粉病的病原体,在其宿主玉米 (Zea mays) 的生物营养生长过程中诱导肿瘤形成。我们在感染后 1 天 (dpi) 和 8 dpi 之间对受感染的叶子进行了综合代谢组和转录组调查,分别代表受感染的叶原基和完全发育的肿瘤。在 4 dpi 和 8 dpi 时,我们观察到与模拟对照组相比,肿瘤中富氮氨基酸谷氨酰胺和天冬酰胺的含量大幅增加,而参与初级氮同化的酶的活性以及氨和硝酸盐的含量降低了 50%。利用稳定同位素标记,我们可以证明玉米淀粉诱导的肿瘤显示出土壤来源的 (NO3-)-N-15 的同化减少,并且代表了强大的氮汇。用[N-15]尿素对系统源叶的游离氨基酸库进行特异性标记,结果显示从系统叶到肿瘤组织的有机氮输入增加,表明有机氮供应支持玉米 U. 玉米诱导的肿瘤的形成。反过来,在受感染的植物中,系统源叶的氨基酸输出量增加了一倍。对韧皮部氨基酸库的分析表明,谷氨酰胺和天冬酰胺不会被转运到肿瘤组织,尽管发现这两种氨基酸在肿瘤内积累。在受感染植物上发生肿瘤后,系统源叶的光合作用增加并且衰老延迟,表明氮库需求的增加可以决定源叶的光合速率。
The basidiomycete Ustilago maydis is the causal agent of corn smut disease and induces tumor formation during biotrophic growth in its host maize (Zea mays). We have conducted a combined metabolome and transcriptome survey of infected leaves between 1 d post infection (dpi) and 8 dpi, representing infected leaf primordia and fully developed tumors, respectively. At 4 and 8 dpi, we observed a substantial increase in contents of the nitrogen-rich amino acids glutamine and asparagine, while the activities of enzymes involved in primary nitrogen assimilation and the content of ammonia and nitrate were reduced by 50% in tumors compared with mock controls. Employing stable isotope labeling, we could demonstrate that U. maydis-induced tumors show a reduced assimilation of soil-derived (NO3-)-N-15 and represent strong sinks for nitrogen. Specific labeling of the free amino acid pool of systemic source leaves with [N-15] urea revealed an increased import of organic nitrogen from systemic leaves to tumor tissue, indicating that organic nitrogen provision supports the formation of U. maydis-induced tumors. In turn, amino acid export from systemic source leaves was doubled in infected plants. The analysis of the phloem amino acid pool revealed that glutamine and asparagine are not transported to the tumor tissue, although these two amino acids were found to accumulate within the tumor. Photosynthesis was increased and senescence was delayed in systemic source leaves upon tumor development on infected plants, indicating that the elevated sink demand for nitrogen could determine photosynthetic rates in source leaves.