The normal growth of Rehmannia glutinosa, a widely used medicinal plant in China, is severely disturbed by replant disease. The formation of replant disease commonly involves interactions among plants, allelochemicals and microbes; however, these relationships remain largely unclear. As a result, no effective measures are currently available to treat replant disease. In this study, an integrated R. glutinosa transcriptome was constructed, from which an R. glutinosa protein library was obtained. iTRAQ technology was then used to investigate changes in the proteins in replanted R. glutinosa roots, and the proteins that were expressed in response to replant disease were identified. An integrated R. glutinosa transcriptome from different developmental stages of replanted and normal-growth R. glutinosa produced 65,659 transcripts, which were accurately translated into 47,818 proteins. Using this resource, a set of 189 proteins was found to be significantly differentially expressed between normal-growth and replanted R. glutinosa. Of the proteins that were significantly upregulated in replanted R. glutinosa, most were related to metabolism, immune responses, ROS generation, programmed cell death, ER stress, and lignin synthesis. By integrating these key events and the results of previous studies on replant disease formation, a new picture of the damaging mechanisms that cause replant disease stress emerged. Replant disease altered the metabolic balance of R. glutinosa, activated immune defence systems, increased levels of ROS and antioxidant enzymes, and initiated the processes of cell death and senescence in replanted R. glutinosa. Additionally, lignin deposition in R. glutinosa roots that was caused by replanting significantly inhibited tuberous root formation. These key processes provide important insights into the underlying mechanisms leading to the formation of replant disease and also for the subsequent development of new control measures to improve production and quality of replanted plants.

Consecutive monoculture practice facilitates enrichment of rhizosphere pathogenic microorganisms and eventually leads to the emergence of replant disease. However, little is known about the interaction relationship among pathogens enriched in rhizosphere soils, Nucleotide binding-leucine-rich repeats (NB-LRR) receptors that specifically recognize pathogens in effector-triggered immunity (ETI) and physiological indicators under replant disease stress in Rehmannia glutinosa. In this study, a controlled experiment was performed using different kinds of soils from sites never planted R. glutinosa (NP), replanted R. glutinosa (TP) and mixed by different ration of TP soils (1/3TP and 2/3TP), respectively. As a result, different levels of TP significantly promoted the proliferation of Fusarium oxysporum f.sp. R. glutinosa (FO). Simultaneously, a comparison between FO numbers and NB-LRR expressions indicated that NB-LRRs were not consecutively responsive to the FO proliferation at transcriptional levels. Further analysis found that NB-LRRs responded to FO invasion with a typical phenomenon of “promotion in low concentration and suppression in high concentration”, and 6 NB-LRRs were identified as candidates for responding R. glutinosa replant disease. Furthermore, four critical hormones of salicylic acid (SA), jasmonic acid (JA), ethylene (ET) and abscisic acid (ABA) had higher levels in 1/3TP, 2/3TP and TP than those in NP. Additionally, increasing extents of SA contents have significantly negative trends with FO changes, which implied that SA might be inhibited by FO in replanted R. glutinosa. Concomitantly, the physiological indexes reacted alters of cellular process regulated by NB-LRR were affected by complex replant disease stresses and exhibited strong fluctuations, leading to the death of R. glutinosa. These findings provide important insights and clues into further revealing the mechanism of R. glutinosa replant disease.

The stem-boring herbivore Aeolesthes induta severely threatens tea (Camellia sinensis) production, yet the systemic defense mechanisms of tea plants remain largely elusive. The unique age-dependent infestation pattern of A. induta—with minimal damage to young tea plants but infestation rates reaching 20% in 30-year-old trees and nearly 100% in ancient tea trees—necessitated field sampling from naturally infested old tea plantations rather than controlled laboratory conditions. By integrating rhizosphere microbiomics, transcriptomics, and multi-omics modeling, this study characterized the defensive regulatory networks of 30-year-old Shuixian tea cultivars under A. induta infestation. Rhizosphere microbiome analysis revealed that herbivore attack significantly reshaped the microbial community structure, reducing bacterial diversity and simplifying co-occurrence network complexity. Transcriptomic and metabolomic profiling demonstrated a precise source–sink defense allocation between host tissues. In leaves acting as the photosynthetic source, metabolic reprogramming was dominated by the systematic accumulation of soluble sugars and sugar acids for systemic energy reallocation. Concurrently, the roots acting as the metabolic sink vigorously activated the jasmonic acid (JA) signaling cascade and upregulated genes enriched in phenylpropanoid biosynthesis and alpha-linolenic acid metabolism. This molecular activation drove the substantial de novo synthesis of defensive phenolic acids, while downregulating growth-related flavonoids. Integrated network modeling further highlighted the phenylpropanoid pathway as the central regulatory node coupling transcript–metabolite fluctuations. This study constructs an integrated soil microbiome–root–leaf defense network, providing novel mechanistic insights into plant–borer interactions and a valuable foundation for future insect-resistant breeding programs in the tea industry.