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Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores.
PLOS Biology ( IF 7.8 ) Pub Date : 2020-08-18 , DOI: 10.1371/journal.pbio.3000830
Suhua Li 1 , Youngsung Joo 1, 2 , Dechang Cao 1, 3 , Ran Li 1, 4 , Gisuk Lee 1, 2 , Rayko Halitschke 1 , Gundega Baldwin 1 , Ian T Baldwin 1 , Ming Wang 1, 5
Affiliation  

Plants are attacked by herbivores, which often specialize on different tissues, and in response, have evolved sophisticated resistance strategies that involve different types of chemical defenses frequently targeted to different tissues. Most known phytohormones have been implicated in regulating these defenses, with jasmonates (JAs) playing a pivotal role in complex regulatory networks of signaling interactions, often generically referred to as “cross talk.” The newly identified class of phytohormones, strigolactones (SLs), known to regulate the shoot architecture, remain unstudied with regard to plant–herbivore interactions. We explored the role of SL signaling in resistance to a specialist weevil (Trichobaris mucorea) herbivore of the native tobacco, Nicotiana attenuata, that attacks the root–shoot junction (RSJ), the part of the plant most strongly influenced by alterations in SL signaling (increased branching). As SL signaling shares molecular components, such as the core F-box protein more axillary growth 2 (MAX2), with another new class of phytohormones, the karrikins (KARs), which promote seed germination and seedling growth, we generated transformed lines, individually silenced in the expression of NaMAX2, dwarf 14 (NaD14: the receptor for SL) and carotenoid cleavage dioxygenase 7 (NaCCD7: a key enzyme in SL biosynthesis), and karrikin insensitive 2 (NaKAI2: the KAR receptor). The mature stems of all transgenic lines impaired in the SL, but not the KAR signaling pathway, overaccumulated anthocyanins, as did the stems of plants attacked by the larvae of weevil, which burrow into the RSJs to feed on the pith of N. attenuata stems. T. mucorea larvae grew larger in the plants silenced in the SL pathway, but again, not in the KAI2-silenced plants. These phenotypes were associated with elevated JA and auxin (indole-3-acetic acid [IAA]) levels and significant changes in the accumulation of defensive compounds, including phenolamides and nicotine. The overaccumulation of phenolamides and anthocyanins in the SL pathway–silenced plants likely resulted from antagonism between the SL and JA pathway in N. attenuata. We show that the repressors of SL signaling, suppressor of max2-like (NaSMXL6/7), and JA signaling, jasmonate zim-domain (NaJAZs), physically interact, promoting NaJAZb degradation and releasing jasmonate insensitive 1 (JIN1/MYC2) (NaMYC2), a critical transcription factor promoting JA responses. However, the increased performance of T. mucorea larvae resulted from lower pith nicotine levels, which were inhibited by increased IAA levels in SL pathway–silenced plants. This inference was confirmed by decapitation and auxin transport inhibitor treatments that decreased pith IAA and increased nicotine levels. In summary, SL signaling tunes specific sectors of specialized metabolism in stems, such as phenylpropanoid and nicotine biosynthesis, by tailoring the cross talk among phytohormones, including JA and IAA, to mediate herbivore resistance of stems. The metabolic consequences of the interplay of SL, JA, and IAA signaling revealed here could provide a mechanism for the commonly observed pattern of herbivore tolerance/resistance trade-offs.



中文翻译:


独脚金内酯信号调节烟草茎中的专门代谢以及与以茎为食的食草动物的相互作用。



植物受到食草动物的攻击,而食草动物通常专门攻击不同的组织,作为回应,植物进化出了复杂的抵抗策略,其中涉及经常针对不同组织的不同类型的化学防御。大多数已知的植物激素都与调节这些防御有关,其中茉莉酸 (JAs) 在信号相互作用的复杂调节网络中发挥着关键作用,通常被称为“串扰”。新发现的一类植物激素——独脚金内酯(SL),已知可以调节芽的结构,但有关植物与食草动物相互作用的研究仍未得到研究。我们探索了 SL 信号在抵抗本地烟草的特异象鼻虫 ( Trichobaris mucorea ) 草食动物(Nicotiana attenuata ) 中的作用,这种动物会攻击根茎连接处 (RSJ),这是植物中受 SL 信号变化影响最强烈的部分(增加分支)。由于 SL 信号传导共享分子成分,例如核心 F-box 蛋白 more axillary Growth 2 (MAX2),与另一类新的植物激素,即 karrikins (KAR),可促进种子发芽和幼苗生长,因此我们分别生成了转化系NaMAX2dwarf 14NaD14 :SL 受体)和类胡萝卜素裂解双加氧酶 7NaCCD7 :SL 生物合成中的关键酶)和karrikin insensitive 2NaKAI2 :KAR 受体)的表达被沉默。所有转基因品系的成熟茎在 SL 中都受到损害,但 KAR 信号通路却没有受到损害,花青素过度积累,就像受到象鼻虫幼虫攻击的植物茎一样,象鼻虫幼虫钻入 RSJ 中以N的髓为食。 茎变细T。毛霉菌幼虫在 SL 途径沉默的植物中长得更大,但在KAI2沉默的植物中则不然。这些表型与 JA 和生长素(吲哚-3-乙酸 [IAA])水平升高以及防御化合物(包括酚酰胺和尼古丁)积累的显着变化相关。 SL 途径沉默植物中酚酰胺和花青素的过度积累可能是由于N中 SL 和 JA 途径之间的拮抗作用造成的。衰减。我们发现 SL 信号传导的阻遏物、max2 样抑制物 (NaSMXL6/7) 和 JA 信号传导、茉莉酸 zim 结构域 (NaJAZ) 发生物理相互作用,促进 NaJAZb 降解并释放茉莉酸不敏感 1 (JIN1/MYC2) (NaMYC2) ),促进 JA 反应的关键转录因子。然而, T的性能有所提高。 mucorea幼虫是由于髓内尼古丁水平较低而产生的,而SL途径沉默植物中IAA水平的增加会抑制这种尼古丁水平。这一推论得到了断头和生长素转运抑制剂治疗的证实,这些治疗降低了髓内 IAA 并增加了尼古丁水平。总之,SL 信号通过调整植物激素(包括 JA 和 IAA)之间的串扰来调节茎中专门代谢的特定部分,例如苯丙素和尼古丁生物合成,以介导茎的食草动物抗性。这里揭示的 SL、JA 和 IAA 信号相互作用的代谢后果可能为常见的草食动物耐受/抗性权衡模式提供一种机制。

更新日期:2020-08-19
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