Systemic long-distance sulfur transport and its role in symbiotic root nodule protein turnover

IF 4 3区 生物学 Q1 PLANT SCIENCES Journal of plant physiology Pub Date : 2024-04-26 DOI:10.1016/j.jplph.2024.154260
Alina Siegl , Leila Afjehi-Sadat , Stefanie Wienkoop
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Abstract

Sulfur is an essential nutrient for all plants, but also crucial for the nitrogen fixing symbiosis between legumes and rhizobia. Sulfur limitation can hamper nodule development and functioning. Until now, it remained unclear whether sulfate uptake into nodules is local or mainly systemic via the roots, and if long-distance transport from shoots to roots and into nodules occurs. Therefore, this work investigates the systemic regulation of sulfur transportation in the model legume Lotus japonicus by applying stable isotope labeling to a split-root system. Metabolite and protein extraction together with mass spectrometry analyses were conducted to determine the plants molecular phenotype and relative isotope protein abundances. Data show that treatments of varying sulfate concentrations including the absence of sulfate on one side of a nodulated root was not affecting nodule development as long as the other side of the root system was provided with sufficient sulfate. Concentrations of shoot metabolites did not indicate a significant stress response caused by a lack of sulfur. Further, we did not observe any quantitative changes in proteins involved in biological nitrogen fixation in response to the different sulfate treatments. Relative isotope abundance of 34S confirmed a long-distance transport of sulfur from one side of the roots to the other side and into the nodules. Altogether, these results provide evidence for a systemic long-distance transport of sulfur via the upper part of the plant to the nodules suggesting a demand driven sulfur distribution for the maintenance of symbiotic N-fixation.

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系统性长距离硫运输及其在共生根瘤蛋白质周转中的作用
硫是所有植物的必需营养元素,也是豆科植物与根瘤菌之间固氮共生的关键。硫限制会阻碍结核的发育和功能。到目前为止,人们还不清楚硫酸盐吸收到结核中是局部的还是主要通过根系进行系统吸收,也不清楚是否会发生从芽到根再到结核的长距离运输。因此,本研究通过对分根系统进行稳定同位素标记,研究了模式豆科植物日本莲的硫运输系统调控。通过代谢物和蛋白质提取以及质谱分析,确定了植物的分子表型和相对同位素蛋白质丰度。数据显示,只要根系的另一侧有足够的硫酸盐,不同硫酸盐浓度的处理,包括一侧根系没有硫酸盐,都不会影响结核的发育。芽代谢物的浓度并不表明缺硫会导致明显的应激反应。此外,我们没有观察到参与生物固氮的蛋白质在不同硫酸盐处理下有任何定量变化。34S 的相对同位素丰度证实了硫从根的一侧向另一侧和结核的长距离运输。总之,这些结果提供了硫通过植物上部向结核进行系统长距离运输的证据,表明硫的分布是由需求驱动的,以维持共生固氮作用。
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来源期刊
Journal of plant physiology
Journal of plant physiology 生物-植物科学
CiteScore
7.20
自引率
4.70%
发文量
196
审稿时长
32 days
期刊介绍: The Journal of Plant Physiology is a broad-spectrum journal that welcomes high-quality submissions in all major areas of plant physiology, including plant biochemistry, functional biotechnology, computational and synthetic plant biology, growth and development, photosynthesis and respiration, transport and translocation, plant-microbe interactions, biotic and abiotic stress. Studies are welcome at all levels of integration ranging from molecules and cells to organisms and their environments and are expected to use state-of-the-art methodologies. Pure gene expression studies are not within the focus of our journal. To be considered for publication, papers must significantly contribute to the mechanistic understanding of physiological processes, and not be merely descriptive, or confirmatory of previous results. We encourage the submission of papers that explore the physiology of non-model as well as accepted model species and those that bridge basic and applied research. For instance, studies on agricultural plants that show new physiological mechanisms to improve agricultural efficiency are welcome. Studies performed under uncontrolled situations (e.g. field conditions) not providing mechanistic insight will not be considered for publication. The Journal of Plant Physiology publishes several types of articles: Original Research Articles, Reviews, Perspectives Articles, and Short Communications. Reviews and Perspectives will be solicited by the Editors; unsolicited reviews are also welcome but only from authors with a strong track record in the field of the review. Original research papers comprise the majority of published contributions.
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