Department of Biology, University of Miami, Coral Gables, Florida, USA.
Department of Earth and Environment, Florida International University, Miami, Florida, USA.
Ecology. 2022 Jun;103(6):e3679. doi: 10.1002/ecy.3679. Epub 2022 Apr 13.
The rapid human-driven changes in the environment during the Anthropocene have placed extreme stress on many plants and animals. Beneficial interactions with microorganisms may be crucial for ameliorating these stressors and facilitating the ecosystem services host organisms provide. Foliar endophytes, microorganisms that reside within leaves, are found in essentially all plants and can provide important benefits (e.g., enhanced drought tolerance or resistance to herbivory). However, it remains unclear how important the legacy effects of the abiotic stressors that select on these microbiomes are for affecting the degree of stress amelioration provided to their hosts. To elucidate foliar endophytes' role in host-plant salt tolerance, especially if salinity experienced in the field selects for endophytes that are better suited to improve the salt tolerance of their hosts, we combined field collections of 90 endophyte communities from 30 sites across the coastal Everglades with a manipulative growth experiment assessing endophyte inoculation effects on host-plant performance. Specifically, we grew >350 red mangrove (Rhizophora mangle) seedlings in a factorial design that manipulated the salinity environment the seedlings experienced (freshwater vs. saltwater), the introduction of field-collected endophytes (live vs. sterilized inoculum), and the legacy of salinity stress experienced by these introduced endophytes, ranging from no salt stress (0 parts per thousand [ppt] salinity) to high salt stress (40 ppt) environments. We found that inoculation with field-collected endophytes significantly increased mangrove performance across almost all metrics examined (15%-20% increase on average), and these beneficial effects typically occurred when the endophytes were grown in saltwater. Importantly, our study revealed the novel result that endophyte-conferred salinity tolerance depended on microbiome salinity legacy in a key coastal foundation species. Salt-stressed mangroves inoculated with endophyte microbiomes from high-salinity environments performed, on average, as well as plants grown in low-stress freshwater, while endophytes from freshwater environments did not relieve host salinity stress. Given the increasing salinity stress imposed by sea level rise and the importance of foundation species like mangroves for ecosystem services, our results indicate that consideration of endophytic associations and their salinity legacy may be critical for the successful restoration and management of coastal habitats.
人类世期间环境的快速人为变化给许多动植物带来了极大的压力。与微生物的有益相互作用对于缓解这些压力源并促进宿主生物提供的生态系统服务可能至关重要。叶内内生菌是生活在叶子内的微生物，几乎存在于所有植物中，它们可以提供重要的益处（例如，增强耐旱性或抗草食性）。然而，仍然不清楚选择这些微生物组的非生物压力的遗留效应对影响为其宿主提供的压力缓解程度有多重要。为了阐明叶内内生菌在宿主植物耐盐性中的作用，特别是如果在田间经历的盐度选择更适合提高宿主耐盐性的内生菌，我们结合了 30 个沿海大沼泽地 30 个地点的 90 个内生菌群落的野外采集，以及评估内生菌接种对宿主植物性能影响的操纵生长实验。具体来说，我们在一个因子设计中种植了超过 350 株红树（Rhizophora mangle）幼苗，该设计操纵了幼苗经历的盐度环境（淡水与盐水）、引入的野外采集内生菌（活的与灭菌的接种物）以及这些引入的内生菌经历的盐度压力的遗留效应，范围从无盐度压力（0 ppt 盐度）到高盐度压力（40 ppt）环境。我们发现，接种野外采集的内生菌显著提高了红树林的性能，几乎所有指标都增加了 15%-20%，而且这些有益影响通常发生在内生菌在盐水中生长时。重要的是，我们的研究揭示了一个新的结果，即内生菌赋予的耐盐性取决于关键沿海基础物种中微生物组的盐度遗留效应。与来自高盐度环境的内生菌微生物组接种的盐胁迫红树林，平均表现与生长在低盐胁迫淡水的植物一样好，而来自淡水环境的内生菌并不能缓解宿主的盐胁迫。考虑到海平面上升带来的盐度压力增加以及红树林等基础物种对生态系统服务的重要性，我们的结果表明，考虑内生关联及其盐度遗留效应可能对沿海栖息地的成功恢复和管理至关重要。
