Yue Hong, Sun Xuming, Wang Tingting, Zhang Ali, Han Dejun, Wei Gehong, Song Weining, Shu Duntao
College of Agronomy, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Northwest A&F University, Yangling, Shaanxi, 712100, China.
College of Life Sciences, National Key Laboratory of Crop Improvement for Stress Tolerance and Production, Northwest A&F University, Yangling, Shaanxi, 712100, China.
Microbiome. 2024 Mar 4;12(1):44. doi: 10.1186/s40168-024-01770-8.
The severity and frequency of drought are expected to increase substantially in the coming century and dramatically reduce crop yields. Manipulation of rhizosphere microbiomes is an emerging strategy for mitigating drought stress in agroecosystems. However, little is known about the mechanisms underlying how drought-resistant plant recruitment of specific rhizosphere fungi enhances drought adaptation of drought-sensitive wheats. Here, we investigated microbial community assembly features and functional profiles of rhizosphere microbiomes related to drought-resistant and drought-sensitive wheats by amplicon and shotgun metagenome sequencing techniques. We then established evident linkages between root morphology traits and putative keystone taxa based on microbial inoculation experiments. Furthermore, root RNA sequencing and RT-qPCR were employed to explore the mechanisms how rhizosphere microbes modify plant response traits to drought stresses.
Our results indicated that host plant signature, plant niche compartment, and planting site jointly contribute to the variation of soil microbiome assembly and functional adaptation, with a relatively greater effect of host plant signature observed for the rhizosphere fungi community. Importantly, drought-resistant wheat (Yunhan 618) possessed more diverse bacterial and fungal taxa than that of the drought-sensitive wheat (Chinese Spring), particularly for specific fungal species. In terms of microbial interkingdom association networks, the drought-resistant variety possessed more complex microbial networks. Metagenomics analyses further suggested that the enriched rhizosphere microbiomes belonging to the drought-resistant cultivar had a higher investment in energy metabolism, particularly in carbon cycling, that shaped their distinctive drought tolerance via the mediation of drought-induced feedback functional pathways. Furthermore, we observed that host plant signature drives the differentiation in the ecological role of the cultivable fungal species Mortierella alpine (M. alpina) and Epicoccum nigrum (E. nigrum). The successful colonization of M. alpina on the root surface enhanced the resistance of wheats in response to drought stresses via activation of drought-responsive genes (e.g., CIPK9 and PP2C30). Notably, we found that lateral roots and root hairs were significantly suppressed by co-colonization of a drought-enriched fungus (M. alpina) and a drought-depleted fungus (E. nigrum).
Collectively, our findings revealed host genotypes profoundly influence rhizosphere microbiome assembly and functional adaptation, as well as it provides evidence that drought-resistant plant recruitment of specific rhizosphere fungi enhances drought tolerance of drought-sensitive wheats. These findings significantly underpin our understanding of the complex feedbacks between plants and microbes during drought, and lay a foundation for steering "beneficial keystone biome" to develop more resilient and productive crops under climate change. Video Abstract.
预计在未来一个世纪，干旱的严重程度和频率将大幅增加，并显著降低作物产量。操纵根际微生物群落是减轻农业生态系统干旱胁迫的一种新兴策略。然而，对于抗旱植物招募特定根际真菌增强干旱敏感小麦干旱适应性的潜在机制，我们知之甚少。在此，我们通过扩增子和鸟枪法宏基因组测序技术，研究了与抗旱和干旱敏感小麦相关的根际微生物群落组装特征和功能概况。然后，基于微生物接种实验，我们建立了根系形态特征与假定关键类群之间的明显联系。此外，利用根系RNA测序和RT-qPCR技术，探索根际微生物改变植物对干旱胁迫响应性状的机制。
我们的结果表明，宿主植物特征、植物生态位隔室和种植地点共同导致土壤微生物群落组装和功能适应性的变化，其中宿主植物特征对根际真菌群落的影响相对更大。重要的是，抗旱小麦（云汉618）比干旱敏感小麦（中国春）拥有更多样化的细菌和真菌类群，特别是对于特定的真菌物种。在微生物跨界关联网络方面，抗旱品种拥有更复杂的微生物网络。宏基因组学分析进一步表明，属于抗旱品种的富集根际微生物群落在能量代谢方面投入更高，特别是在碳循环方面，通过干旱诱导的反馈功能途径的介导，形成了它们独特的耐旱性。此外，我们观察到宿主植物特征驱动了可培养真菌物种高山被孢霉（M. alpina）和黑附球菌（E. nigrum）生态作用的分化。高山被孢霉在根表面的成功定殖通过激活干旱响应基因（如CIPK9和PP2C30）增强了小麦对干旱胁迫的抗性。值得注意的是，我们发现，富含干旱真菌（高山被孢霉）和缺乏干旱真菌（黑附球菌）的共同定殖显著抑制了侧根和根毛的生长。
总体而言，我们的研究结果表明宿主基因型深刻影响根际微生物群落组装和功能适应性，同时也提供了证据，证明抗旱植物招募特定根际真菌可增强干旱敏感小麦的耐旱性。这些发现显著加强了我们对干旱期间植物与微生物之间复杂反馈的理解，并为引导“有益关键生物群落”以在气候变化下培育更具韧性和生产力的作物奠定了基础。视频摘要。
