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Post-herbivory Tea Plant Leaves Restructure Endophytic Microbiota to Resist Disease and Boost Saccharide Metabolism to Promote Growth

ABSTRACT:

The induced capacity of plant growth-defense trade-offs under biotic stress is increasingly recognized. While many studies mainly focus on plants’ defense activation stage during insect attacks, limited attention has been given to post-stress recovery. Herein, leaves from normal and post-herbivory tea plants were collected during the compensation stage, and their microbiomes, metabolomes, and transcriptomes were used to dissect the mechanisms underlying growth-defense trade-offs. The results revealed that apart from altering the microbial community diversity, insect herbivory significantly enriched leaf-associated pathogens, particularly Alternaria spp. Network analysis and in-situ separation jointly revealed the role of Sphingomonas aquatilis in resisting pathogen invasion. Meanwhile, the restructured microbiota exhibited stronger network stability, indicating the enhancement of pathogen resistance among the endophytic community. Moreover, we found that downregulated flavonoids were defense compounds against pathogens and upregulated saccharides were plant growth-promoting compounds, which were verified in subsequent tests. Overall, tea plants compensate for reduced defense through restructuring of the endophytic microbiota, and prioritize growth over defense through metabolic resetting after insect herbivory. This study also revealed new biocontrol and growth-promoting resources for tea plants.

INSTRUMENT(S): Liquid Chromatography MS - positive - HILIC, Liquid Chromatography MS - negative - HILIC

PROVIDER: MTBLS12664 | MetaboLights | 2025-07-02

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS12664_LC-MS_negative_hilic_metabolite_profiling.txt	Txt
	a_MTBLS12664_LC-MS_positive_hilic_metabolite_profiling.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS12664_LC-MS_negative_hilic_metabolite_profiling_v2_maf.tsv	Tabular
	m_MTBLS12664_LC-MS_positive_hilic_metabolite_profiling_v2_maf.tsv	Tabular

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Project description:<p>Entomopathogenic fungi have the ability to both directly kill insect pests and act as plant endophytic fungi to impact plant growth and development. Despite this, the widespread endophytic use of these fungi in tea plants (Camellia sinensis) is still limited. This study examined how Beauveria bassiana colonizes tea plant tissues and its impact on tea plant growth and development. Through amplicon sequencing and liquid chromatography-tandem mass spectrometry (LC-MS/MS), the study investigated the response patterns of dominant endophytic microbial populations in tea plants during fungal colonization and the alterations in secondary metabolites in tea plants due to the colonization process. B. bassiana effectively colonized tea seedlings through root irrigation and foliar spraying methods, showing a preference for stems, and the colonization persisted for more than 90 days. Colonization resulted in a reduction in the diversity and structural stability of the endophytic microbial community in tea plants; however, it also enhanced the importance of ecologically mutualistic relationships or cooperative interactions in community assembly. Additionally, colonization had a more pronounced effect on endophytic fungi compared to endophytic bacteria. It led to an increase in the relative abundance of arbuscular mycorrhizal fungi in root tissues and a decrease in the relative abundance of total plant pathogens in tea plant tissues. Terpenoids were the most significantly associated differential metabolites following B. bassiana colonization, followed by steroids and their derivatives, and flavonoids. Colonization by B. bassiana resulted in elevated levels of the majority of differential metabolites in tea plant stems at the onset of colonization. The colonization of B. bassiana in tea plants displayed a strong positive correlation with 26 distinct metabolites, such as proanthocyanidin B2 and L-malic acid. This colonization altered the endophytic microbial community, impacting metabolic pathways associated with plant hormone synthesis, volatile compound production, as well as the growth, development, and defense of tea plants.</p>

Project description:In plants, an increase in resource allocation to growth (primary metabolism) associated with the presence of neighbors is likely to reduce defense-related production (secondary metabolism), making plants more vulnerable to herbivory. Even though there is increasing evidence supporting this “trade-off hypothesis”, the underlying mechanisms are still unclear. Far red (FR) radiation reflected from plant tissues serves as an early warning signal of future competition, triggering a suite of plastic morphological adjustments that improve plant’s ability to compete for light in crowded populations. Recent evidence from our lab showed that, when competition signals are present, plant defenses are severely reduced. Besides direct effects of herbivory and competition signals on target plants, second order effects occurs on neighboring plants through plant volatiles (PVs) communication. PVs play a key role in plant-plant and plant-insect interactions, changing its content and composition in response to environmental conditions. To increase our understanding of the molecular mechanisms underlying those interacting signaling webs, we performed a field study with tomato plants (cv Moneymaker), in which plants of EMITTER plots (six plants plot-1) were subjected to herbivory (nine larvae of Spodoptera eridania plant-1) and competition signals (increased FR radiation) in a factorial design. Light treatment started 28 days after sowing (DAS), and herbivory treatment and volatiles conduction started 34 DAS. Volatiles were conducted from EMITTER to RECEIVER plots (five plants plot-1) using a 5 inch, 1.4 m long tube fitted with a computer-type fan. 40 and 45 DAS, larval performance was measured on EMITTER plots as well as naturally-occurring insect colonization on RECEIVER plots. Finally (46 DAS), samples for bulk phenolic content were taken on every plot, and plant material from 4th and 5th leaves was collected for microarray analysis. There were three real biological replicates. Keywords: Reference design

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Post-herbivory Tea Plant Leaves Restructure Endophytic Microbiota to Resist Disease and Boost Saccharide Metabolism to Promote Growth

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