2.2  Wired connections between independent plants via Dodder-mediated interspecific signaling
Dodder is a plant holoparasite that acquires water and nutrients from host plants via the haustorium, which physically connects the parasite to its host. Dodder species have broad host range, and can interconnect several plant species or clusters of the same species (Figure 1) to generate a common dodder network. The common dodder network can be considered as an inter-plant highway that translocates large numbers of proteins, RNA, metabolites, and plant viruses over a distance of at least 100 cm (Hettenhausen et al. , 2017, Zhuang, Li, Song, Hettenhausen, Schuman, Sun, Zhang, Li, Song & Wu, 2018). The common dodder network can translocate more than 1,500 proteins between soybean and Arabidopsis, and some of these proteins can localize in dodder seeds. Approximately 15–30% of dodder proteins have host origin, including transcription factors and R proteins that may function in signal transaction. Dodder proteins can transfer to host plant cells.
Plants can anticipate future threats by receiving neighboring plant signals transferred through the common dodder network. Although there are few reports on the role of the common dodder network in inter-plant signaling, the results indicate that these transferred signals are important in biotic/abiotic stress responses. When a host of dodder plant is under abiotic stress such high salinity, dodder transfers salinity stress signals through a cluster of plants at a rate of 1.2 cm per min, which prime salt tolerance in neighboring receiver plants. This receiver plant priming changes the transcriptome, proline levels, and stomatal conduction, so that the receiver plant stress response becomes similar to that of the donor plant (Li, Zhang, Liu, Liu, Shen, Zhuang & Wu, 2020b).
Plants infected with different herbivorous insects transfer relatively long-distance signals to conspecific and heterospecific neighbors via the common dodder network (Hettenhausen et al. , 2017, Zhuanget al. , 2018). Myzus persica infestation reduces the contents of salicylic acid (SA) and jasmonic acid (JA) in dodder by up to 58% and 41%, respectively. Aphids can modulate hormonal signaling by injecting effector proteins into dodder plants (Rodriguez & Bos, 2013). Aphid-infested dodder induce JA but not SA in soybean hosts, and subsequent phloem sap feeding by M. persica and chewing bySpodoptera litura causes 41% and 20% less damage, respectively, in dodder-infected plants than in control plants. Dodder transfers signals from insect-damaged soybean to conspecific or heterospecific plants, such as tomato and Arabidopsis. Gene expression and RNA-seq analyses reveal intense transcriptome modification in receiver plants. An unknown signal can translocate between common dodder network–connected Arabidopsis plants at a rate of 1 cm/min. A wave of signal transduction propagated between connected Arabidopsis plants, as intracellular WRKY 40 and WRKY53 transcription factors reached maximum expression at 45 and 90 min after donor plant damage in the second and fourth plants in the cluster, respectively (Zhuang et al. , 2018).