Table_4_Belowground Chemical Interactions: An Insight Into Host-Specific Behavior of Globodera spp. Hatched in Root Exudates From Potato and Its Wild Relative, Solanum sisymbriifolium.XLSX

Understanding belowground chemical interactions between plant roots and plant-parasitic nematodes is immensely important for sustainable crop production and soilborne pest management. Due to metabolic diversity and ever-changing dynamics of root exudate composition, the impact of only certain molecules, such as nematode hatching factors, repellents, and attractants, has been examined in detail. Root exudates are a rich source of biologically active compounds, which plants use to shape their ecological interactions. However, the impact of these compounds on nematode parasitic behavior is poorly understood. In this study, we specifically address this knowledge gap in two cyst nematodes, Globodera pallida, a potato cyst nematode and the newly described species, Globodera ellingtonae. Globodera pallida is a devastating pest of potato (Solanum tuberosum) worldwide, whereas potato is a host for G. ellingtonae, but its pathogenicity remains to be determined. We compared the behavior of juveniles (J2s) hatched in response to root exudates from a susceptible potato cv. Desirée, a resistant potato cv. Innovator, and an immune trap crop Solanum sisymbriifolium (litchi tomato – a wild potato relative). Root secretions from S. sisymbriifolium greatly reduced the infection rate on a susceptible host for both Globodera spp. Juvenile motility was also significantly influenced in a host-dependent manner. However, reproduction on a susceptible host from juveniles hatched in S. sisymbriifolium root exudates was not affected, nor was the number of encysted eggs from progeny cysts. Transcriptome analysis by using RNA-sequencing (RNA-seq) revealed the molecular basis of root exudate-mediated modulation of nematode behavior. Differentially expressed genes are grouped into two major categories: genes showing characteristics of effectors and genes involved in stress responses and xenobiotic metabolism. To our knowledge, this is the first study that shows genome-wide root exudate-specific transcriptional changes in hatched preparasitic juveniles of plant-parasitic nematodes. This research provides a better understanding of the correlation between exudates from different plants and their impact on nematode behavior prior to the root invasion and supports the hypothesis that root exudates play an important role in plant-nematode interactions.

解析植物根系与植物寄生线虫（plant-parasitic nematodes）之间的地下化学互作，对于作物可持续生产及土传害虫治理具有至关重要的意义。由于根系分泌物（root exudate）组分兼具代谢多样性与动态变化特征，目前仅针对线虫孵化因子、驱避剂、引诱剂等少数活性分子的调控作用开展了深入解析。根系分泌物是生物活性化合物的丰富来源，植物可通过其调控自身的生态互作过程。然而，此类化合物对线虫寄生行为的影响仍有待深入阐明。本研究针对两种孢囊线虫展开研究，以填补该领域的认知空白：其一为马铃薯孢囊线虫（Globodera pallida），其二为新定名的Ellington孢囊线虫（Globodera ellingtonae）。马铃薯孢囊线虫是全球范围内危害马铃薯（Solanum tuberosum）的毁灭性害虫；而Ellington孢囊线虫虽可侵染马铃薯，但其致病性尚未明确。本研究比较了分别经易感马铃薯品种'Desirée'、抗病马铃薯品种'Innovator'以及免疫诱集作物荔枝番茄（Solanum sisymbriifolium，马铃薯野生近缘种）根系分泌物孵化的二龄幼虫（J2）的行为特征。荔枝番茄的根系分泌物可显著降低两种孢囊线虫在易感寄主上的侵染率。二龄幼虫的活动能力也呈现出显著的寄主依赖性变化。但经荔枝番茄根系分泌物孵化的幼虫在易感寄主上的繁殖能力并未受到影响，其子代孢囊的含卵量亦无显著差异。本研究通过RNA测序（RNA-seq）开展转录组分析，揭示了根系分泌物介导的线虫行为调控的分子机制。差异表达基因可分为两大类：具备效应蛋白特征的基因，以及参与应激响应与异生物质代谢的基因。据我们所知，本研究首次揭示了植物寄生线虫孵化后的预寄生二龄幼虫中，根系分泌物特异性的全基因组转录水平变化。本研究增进了我们对不同植物根系分泌物与线虫根系入侵前行为影响之间关联的认知，并验证了"根系分泌物在植物-线虫互作中发挥重要作用"这一假说。