Yuan Yuan Song

Interplant Communication of Tomato Plants through Underground Common Mycorrhizal Networks

Plants can defend themselves to pathogen and herbivore attack by responding to chemical signals that are emitted by attacked plants. It is well established that such signals can be transferred through the air. In theory, plants can also communicate with each other through underground common mycorrhizal networks (CMNs) that interconnect roots of multiple plants. However, until now research focused on plant-to-plant carbon nutrient movement and there is no evidence that defense signals can be exchanged through such mycorrhizal hyphal networks. Here, we show that CMNs mediate plant-plant communication between healthy plants and pathogen-infected tomato plants (Lycopersicon esculentum Mill.). After establishment of CMNs with the arbuscular mycorrhizal fungus Glomus mosseae between tomato plants, inoculation of ‘donor’ plants with the pathogen Alternaria solani led to increases in disease resistance and activities of the putative defensive enzymes, peroxidase, polyphenol oxidase, chitinase, β-1,3-glucanase, phenylalanine ammonia-lyase and lipoxygenase in healthy neighbouring ‘receiver’ plants. The uninfected ‘receiver’ plants also activated six defence-related genes when CMNs connected ‘donor’ plants challenged with A. solani. This finding indicates that CMNs may function as a plant-plant underground communication conduit whereby disease resistance and induced defence signals can be transferred between the healthy and pathogen-infected neighbouring plants, suggesting that plants can ‘eavesdrop’ on defence signals from the pathogen-challenged neighbours through CMNs to activate defences before being attacked themselves.

Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon

Significance Silicon (Si) is the second most abundant element in soil, and it can increase plant resistance against many abiotic and biotic stresses. The jasmonate (JA) signaling pathway plays a crucial role in mediating antiherbivore defense responses in plants. Our work shows that Si primes JA-mediated antiherbivore defense responses and increases rice resistance to the leaffolder caterpillar and that Si accumulation in rice leaves is mediated by the JA pathway, suggesting a strong interaction between Si and JA in rice defense against insect herbivores. This interaction may represent a widespread mechanism by which Si enhances plant resistance against biotic stresses in Si-accumulating plants. Although the function of silicon (Si) in plant physiology has long been debated, its beneficial effects on plant resistance against abiotic and biotic stresses, including insect herbivory, have been well documented. In addition, the jasmonate (JA) signaling pathway plays a crucial role in mediating antiherbivore defense responses in plants. However, potential interactions between JA and Si in response to insect attack have not been examined directly. To explore the role JA may play in Si-enhanced resistance, we silenced the expression of allene oxide synthase (OsAOS; active in JA biosynthesis) and CORONATINE INSENSITIVE1 (OsCOI1; active in JA perception) genes in transgenic rice plants via RNAi and examined resulting changes in Si accumulation and defense responses against caterpillar Cnaphalocrocis medinalis (rice leaffolder, LF) infestation. Si pretreatment increased rice resistance against LF larvae in wild-type plants but not in OsAOS and OsCOI1 RNAi lines. Upon LF attack, wild-type plants subjected to Si pretreatment exhibited enhanced defense responses relative to untreated controls, including higher levels of JA accumulation; increased levels of transcripts encoding defense marker genes; and elevated activities of peroxidase, polyphenol oxidase, and trypsin protease inhibitor. Additionally, reduced Si deposition and Si cell expansion were observed in leaves of OsAOS and OsCOI1 RNAi plants in comparison with wild-type plants, and reduced steady-state transcript levels of the Si transporters OsLsi1, OsLsi2, and OsLsi6 were observed in Si-pretreated plants after LF attack. These results suggest a strong interaction between Si and JA in defense against insect herbivores involving priming of JA-mediated defense responses by Si and the promotion of Si accumulation by JA.

Silencing COI1 in Rice Increases Susceptibility to Chewing Insects and Impairs Inducible Defense

The jasmonic acid (JA) pathway plays a key role in plant defense responses against herbivorous insects. CORONATINE INSENSITIVE1 (COI1) is an F-box protein essential for all jasmonate responses. However, the precise defense function of COI1 in monocotyledonous plants, especially in rice (Oryza sativa L.) is largely unknown. We silenced OsCOI1 in rice plants via RNA interference (RNAi) to determine the role of OsCOI1 in rice defense against rice leaf folder (LF) Cnaphalocrocis medinalis, a chewing insect, and brown planthopper (BPH) Nilaparvata lugens, a phloem-feeding insect. In wild-type rice plants (WT), the transcripts of OsCOI1 were strongly and continuously up-regulated by LF infestation and methyl jasmonate (MeJA) treatment, but not by BPH infestation. The abundance of trypsin protease inhibitor (TrypPI), and the enzymatic activities of polyphenol oxidase (PPO) and peroxidase (POD) were enhanced in response to both LF and BPH infestation, but the activity of lipoxygenase (LOX) was only induced by LF. The RNAi lines with repressed expression of OsCOI1 showed reduced resistance against LF, but no change against BPH. Silencing OsCOI1 did not alter LF-induced LOX activity and JA content, but it led to a reduction in the TrypPI content, POD and PPO activity by 62.3%, 48.5% and 27.2%, respectively. In addition, MeJA-induced TrypPI and POD activity were reduced by 57.2% and 48.2% in OsCOI1 RNAi plants. These results suggest that OsCOI1 is an indispensable signaling component, controlling JA-regulated defense against chewing insect (LF) in rice plants, and COI1 is also required for induction of TrypPI, POD and PPO in rice defense response to LF infestation.

Priming of Anti-Herbivore Defense in Tomato by Arbuscular Mycorrhizal Fungus and Involvement of the Jasmonate Pathway

Mycorrhizas play a vital role in soil fertility, plant nutrition, and resistance to environmental stresses. However, mycorrhizal effects on plant resistance to herbivorous insects and the related mechanisms are poorly understood. This study evaluated effects of root colonization of tomato (Solanum lycopersicum Mill.) by arbuscular mycorrhizal fungi (AMF) Glomus mosseae on plant defense responses against a chewing caterpillar Helicoverpa arimigera. Mycorrhizal inoculation negatively affected larval performance. Real time RT-PCR analyses showed that mycorrhizal inoculation itself did not induce transcripts of most genes tested. However, insect feeding on AMF pre-inoculated plants resulted in much stronger defense response induction of four defense-related genes LOXD, AOC, PI-I, and PI-II in the leaves of tomato plants relative to non-inoculated plants. Four tomato genotypes: a wild-type (WT) plant, a jasmonic acid (JA) biosynthesis mutant (spr2), a JA-signaling perception mutant (jai1), and a JA-overexpressing 35S::PS plant were used to determine the role of the JA pathway in AMF-primed defense. Insect feeding on mycorrhizal 35S::PS plants led to higher induction of defense-related genes relative to WT plants. However, insect feeding on mycorrhizal spr2 and jai1 mutant plants did not induce transcripts of these genes. Bioassays showed that mycorrhizal inoculation on spr2 and jai1 mutants did not change plant resistance against H. arimigera. These results indicates that mycorrhizal colonization could prime systemic defense responses in tomato upon herbivore attack, and that the JA pathway is involved in defense priming by AMF.

Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks

Extensive regions of interior Douglas-fir (Pseudotsuga menziesii var. glauca, IDF) forests in North America are being damaged by drought and western spruce budworm (Choristoneura occidentalis). This damage is resulting from warmer and drier summers associated with climate change. To test whether defoliated IDF can directly transfer resources to ponderosa pine (Pinus ponderosae) regenerating nearby, thus aiding in forest recovery, we examined photosynthetic carbon transfer and defense enzyme response. We grew pairs of ectomycorrhizal IDF ‘donor’ and ponderosa pine ‘receiver’ seedlings in pots and isolated transfer pathways by comparing 35 μm, 0.5 μm and no mesh treatments; we then stressed IDF donors either through manual defoliation or infestation by the budworm. We found that manual defoliation of IDF donors led to transfer of photosynthetic carbon to neighboring receivers through mycorrhizal networks, but not through soil or root pathways. Both manual and insect defoliation of donors led to increased activity of peroxidase, polyphenol oxidase and superoxide dismutase in the ponderosa pine receivers, via a mechanism primarily dependent on the mycorrhizal network. These findings indicate that IDF can transfer resources and stress signals to interspecific neighbors, suggesting ectomycorrhizal networks can serve as agents of interspecific communication facilitating recovery and succession of forests after disturbance.

Simulated Acid Rain Accelerates Litter Decomposition and Enhances the Allelopathic Potential of the Invasive Plant Wedelia trilobata (Creeping Daisy)

Abstract Invasive species and acid rain cause global environmental problems. Creeping daisy, an invasive exotic allelopathic weed, has caused great damage in southern China, where acid rain is prevalent. The impact of the acidity of simulated acid rain (SAR) on soil nutrients, the decomposition of creeping daisy litter, and on the allelopathic potential of the surrounding soils was investigated. Litter was treated with SAR at different acidity (pH 2.5, 4.0, 5.6) or with water (pH 7.0) as a control. After 70 d, the remaining amount of creeping daisy litter, nutrient contents, and allelopathic potentials in the surrounding soil were determined. The litter decomposition was commensurate to the increase in the acidity of the SAR. Total C and N contents, NO3−-N and available P increased, levels of NH4+-N, the ratio of C/N and soil pH values decreased, water contents increased and then decreased, whereas available K did not significantly change in the soil surrounding the litters in response to the increase in the acidity of the SAR. Bioassays showed that SAR promoted the allelopathic activity in the soil surrounding the litter, as measured by seedling growth of turnip and radish. In conclusion, our results indicated that SAR influenced soil nutrient status, accelerated creeping daisy litter decomposition, and enhanced the allelopathic potential of its litter in the surrounding soil, suggesting that acid rain may enhance the invasiveness of creeping daisy plants. Nomenclature: Creeping daisy, Wedelia trilobata (L.) Hitchc.; turnip, Brassica campestris L.; radish, Raphanus sativus L.

Resource Transfer Between Plants Through Ectomycorrhizal Fungal Networks

Carbon (C), nutrients and water (H2O) have been known for five decades to flow between plants through ectomycorrhizal (EM) networks. This flux has the potential to affect plant and fungal performance and resource distribution within communities. We asked two questions: (1) What are the pathways and mechanisms for C, nutrient and H2O fluxes between plants through EM networks? (2) What are the magnitude, fate and importance of C, nutrient and H2O transfer among EM plants? Mycorrhizal networks provide a distinct pathway for resource fluxes among plants and mycorrhizal fungi, partitioning them away from other competing soil microbes and plant roots in the soil matrix, and potentially providing a competitive advantage (or disadvantage) for some individuals involved in the network. Carbon and nutrients flow symplastically and apoplastically through mycorrhizal symbionts, hyphae and rhizomorphs along source-sink gradients across the networking mycelia and plant community. EM networks can also facilitate the hydraulic redistribution of soil or plant water following water potential gradients. Carbon fluxes through EM networks have been shown to supply 0–10 % of autotrophic, up to 85 % of partial myco-heterotrophic (MH), and 100 % of fully MH plant C. This C supply has been loosely associated with the increased survival and growth of autotrophic plants, but has been shown to be essential for the survival of MH plants. Network-mediated nitrogen (N) fluxes between N2-fixing and non-N2-fixing plants have supplied up to 40 % of receiver N, and this has been associated with increased plant productivity. Fluxes between non-N2-fixing plants have supplied <5 % of receiver N. Hydraulic redistribution involving EM fungi has supplied up to 50 % of plant water; this has been shown as essential for plant survival in some cases. However, uncertainty remains as to how much of this water transfers through EM networks. Phosphorus transfer through EM networks has not been adequately demonstrated. Overall, this review chapter shows that resource fluxes though EM networks are sufficiently large in some cases to facilitate plant establishment and growth. Resource fluxes through EM networks may thus serve as a method for interactions and cross-scale feedbacks in the development of plant-microbial communities. The outcome of resource transfer through EM networks for the stability of terrestrial ecosystems depends upon the environmental context.

Interactions between Nitrogen and Silicon in Rice and Their Effects on Resistance toward the Brown Planthopper Nilaparvata lugens

Nitrogen (N) and silicon (Si) are two important nutritional elements required for plant growth, and both impact host plant resistance toward insect herbivores. The interaction between the two elements may therefore play a significant role in determining host plant resistance. We investigated this interaction in rice (Oryza sativa L.) and its effect on resistance to the herbivore brown planthopper Nilaparvata lugens (BPH). Our results indicate that high-level (5.76 mM) N fertilization reduced Si accumulation in rice leaves, and furthermore, this decrease was likely due to decreased expression of Si transporters OsLsi1 and OsLsi2. Conversely, reduced N accumulation was observed at high N fertilization levels when Si was exogenously provided, and this was associated with down-regulation of OsAMT1;1 and OsGS1;1, which are involved in ammonium uptake and assimilation, respectively. Under lower N fertilization levels (0.72 and/or 1.44 mM), Si amendment resulted in increased OsNRT1:1, OsGS2, OsFd-GOGAT, OsNADH-GOGAT2, and OsGDH2 expression. Additionally, bioassays revealed that high N fertilization level significantly decreased rice resistance to BPH, and the opposite effect was observed when Si was provided. These results provide additional insight into the antagonistic interaction between Si and N accumulation in rice, and the effects on plant growth and susceptibility to herbivores.