Ancient duplications, multidimensional specializations, and defense role of hexokinases in wheat

IF 6.2 1区 生物学 Q1 PLANT SCIENCES
Xiaolin Tian, Fan Li, Jie Lin, Yun Xu, Kai Tian, Lihua Gu, Yanfeng Zhang, Jin-Rong Xu, Qinhu Wang
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Abstract

Hexokinases (HXKs), which sense and catalyze cellular sugar, play a critical role in the growth and development of various plants, including wheat, a primary source of human calories frequently attacked by fungal pathogens. However, the evolutionary dynamics and functional diversification of HXKs in wheat, particularly their roles in plant defense, remain unclear. Here, we discovered that the wheat hexokinase gene family originated through multiple ancient gene duplications across different plant lineages and has undergone comprehensive, multidimensional functional specialization in gene expression, subcellular localization, enzyme activity, and regulation of plant defense responses. Gene expression analysis suggests that two-thirds of the TaHXK genes are responsive to fungal infection. Subcellular analysis reveals that while six TaHXKs are localized in mitochondria, three TaHXKs from different phylogenetic branches are sorted into other cellular compartments. Notably, biochemical analysis shows that TaHXKs in mitochondria differ in their glucose-catalyzing activity, with TaHXK5 and TaHXK3 exhibiting the highest and lowest enzyme activity, respectively. Consistently, transient expression analysis suggests that TaHXK5 induces various plant defense responses, while TaHXK3 is defective in activating some plant defense responses. Furthermore, inactivation of the glucokinase activity of TaHXK5 compromised its function in defense activation, suggesting that mitochondrial TaHXKs display functional divergence in both enzyme activity and defense-inducing activity that are intrinsically connected. Overall, our findings reveal that the multidimensional specialization events following the ancient duplication events may have shaped the functional diversity of HXKs in wheat, shedding light on their evolutionary dynamics and potentially contributing to the improvement of wheat defense.

小麦中 hexokinases 的古老复制、多维特化和防御作用。
六磷酸酶(HXKs)能感知和催化细胞糖分,在各种植物的生长发育过程中发挥着至关重要的作用,其中包括经常受到真菌病原体侵袭的人类主要热量来源--小麦。然而,小麦中 HXKs 的进化动态和功能多样化,特别是它们在植物防御中的作用,仍然不清楚。在这里,我们发现小麦己糖激酶基因家族起源于不同植物品系的多个古老基因重复,并在基因表达、亚细胞定位、酶活性和植物防御反应调控等方面经历了全面、多维的功能特化。基因表达分析表明,三分之二的 TaHXK 基因对真菌感染有反应。亚细胞分析表明,6 个 TaHXK 定位于线粒体,而来自不同系统发育分支的 3 个 TaHXK 则被分类到其他细胞区。值得注意的是,生化分析表明,线粒体中的 TaHXKs 在葡萄糖催化活性方面存在差异,其中 TaHXK5 和 TaHXK3 的酶活性分别最高和最低。同样,瞬时表达分析表明,TaHXK5 能诱导各种植物防御反应,而 TaHXK3 在激活某些植物防御反应方面存在缺陷。此外,使 TaHXK5 的葡萄糖激酶活性失活会影响其在防御激活中的功能,这表明线粒体 TaHXKs 在酶活性和防御诱导活性方面存在功能差异,而这两者之间存在内在联系。总之,我们的发现揭示了古代复制事件之后的多维特化事件可能塑造了小麦中 HXKs 的功能多样性,揭示了它们的进化动态,并可能有助于提高小麦的防御能力。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
The Plant Journal
The Plant Journal 生物-植物科学
CiteScore
13.10
自引率
4.20%
发文量
415
审稿时长
2.3 months
期刊介绍: Publishing the best original research papers in all key areas of modern plant biology from the world"s leading laboratories, The Plant Journal provides a dynamic forum for this ever growing international research community. Plant science research is now at the forefront of research in the biological sciences, with breakthroughs in our understanding of fundamental processes in plants matching those in other organisms. The impact of molecular genetics and the availability of model and crop species can be seen in all aspects of plant biology. For publication in The Plant Journal the research must provide a highly significant new contribution to our understanding of plants and be of general interest to the plant science community.
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