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Plant-mediated interactions between herbivores play an important role in regulating the composition of herbivore community. The fall armyworm (FAW), Spodoptera frugiperda, which has become one of the most serious pests on corn in China since it invaded in 2018, has been found feeding rice in the field. However, how FAW interacts with native rice insect pests remains largely unknown. Here, we investigated the interaction between FAW and a resident herbivore, striped stem borer (SSB, Chilo suppressalis) on rice. The infestation of rice leaf sheaths (LSs) by SSB larvae systemically enhanced the level of jasmonic acid (JA), abscisic acid (ABA), and trypsin proteinase inhibitors (TPIs), reduced relative water content (RWC) in leaf blades (LBs), and suppressed the growth of FAW larvae. In contrast, because FAW larvae infested LBs and did not affect defence responses in LSs, they did not influence the performance of SSB larvae. Using different mutants, together with bioassays and chemical analysis, we revealed that SSB-induced suppression of FAW larvae growth depended on both the SSB-activated JA pathway and RWC in LBs, whereas the ABA pathway activated by SSB larvae promoted the growth of FAW larvae by impeding water loss. These results provide new insights into mechanisms underlying plant-mediated interactions between herbivores.

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To successfully survive, develop, grow and reproduce, multicellular organisms must coordinate their molecular, physiological, developmental and metabolic responses among their different cells and tissues. This process is mediated by cell-to-cell, vascular and/or volatile communication, and involves electric, chemical and/or hydraulic signals. Within this context, stomata serve a dual role by coordinating their responses to the environment with their neighbouring cells at the epidermis, but also with other stomata present on other parts of the plant. As stomata represent one of the most important conduits between the plant and its above-ground environment, as well as directly affect photosynthesis, respiration and the hydraulic status of the plant by controlling its gas and vapour exchange with the atmosphere, coordinating the overall response of stomata within and between different leaves and tissues plays a cardinal role in plant growth, development and reproduction. Here, we discuss different examples of local and systemic stomatal coordination, the different signalling pathways that mediate them, and the importance of systemic stomatal coordination to our food supply, ecosystems and weather patterns, under our changing climate. We further discuss the potential biotechnological implications of regulating systemic stomatal responses for enhancing agricultural productivity in a warmer and CO2 -rich environment.

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Chitin is a well-known elicitor of disease resistance and its recognition by plants is crucial to perceive fungal infections. Chitin can induce both a local immune response and a systemic disease resistance when provided as a supplement in soils. Unlike local immune responses, it is poorly explored how chitin-induced systemic disease resistance is developed. In this study, we report the systemic induction of disease resistance against the fungal pathogen Bipolaris oryzae by chitin supplementation of soils in rice. The transcriptome analysis uncovered genes related to cell-wall biogenesis, cytokinin signaling, regulation of phosphorylation, and defence priming in the development of chitin-induced systemic response. Alterations of cell-wall composition were observed in leaves of rice plants grown in chitin-supplemented soils, and the disease resistance against B. oryzae was increased in rice leaves treated with a cellulose biosynthesis inhibitor. The disruption of genes for lysin motif (LysM)-containing chitin receptors, OsCERK1 (Chitin elicitor receptor kinase 1) and OsCEBiP (Chitin elicitor-binding protein), compromised chitin-induced systemic disease resistance against B. oryzae and differential expression of chitin-induced genes found in wild-type rice plants. These findings suggest that chitin-induced systemic disease resistance in rice is caused by a perturbation of cell-wall biogenesis in leaves through long-distance signalling after local recognition of chitins by OsCERK1 and OsCEBiP.

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In legumes interacting with rhizobia, the formation of symbiotic organs involved in the acquisition of atmospheric nitrogen gas (N2) is dependent on the plant nitrogen (N) demand. We used Medicago truncatula plants cultivated in split-root systems to discriminate between responses to local and systemic N signaling. We evidenced a strong control of nodule formation by systemic N signaling but obtained no clear evidence of a local control by mineral nitrogen. Systemic signaling of the plant N demand controls numerous transcripts involved in root transcriptome reprogramming associated with early rhizobia interaction and nodule formation. SUPER NUMERIC NODULES (SUNN) has an important role in this control, but we found that major systemic N signaling responses remained active in the sunn mutant. Genes involved in the activation of nitrogen fixation are regulated by systemic N signaling in the mutant, explaining why its hypernodulation phenotype is not associated with higher nitrogen fixation of the whole plant. We show that the control of transcriptome reprogramming of nodule formation by systemic N signaling requires other pathway(s) that parallel the SUNN/CLE (CLAVATA3/EMBRYO SURROUNDING REGION-LIKE PEPTIDES) pathway.

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Forisomes are giant fusiform protein complexes composed of sieve element occlusion (SEO) protein monomers, exclusively found in sieve elements (SEs) of legumes. Forisomes block the phloem mass flow by a Ca2+-induced conformational change (swelling and rounding). We studied the forisome reactivity in four different legume species-Medicago sativa, Pisum sativum, Trifolium pratense and Vicia faba. Depending on the species, we found direct relationships between SE diameter, forisome surface area and distance from the leaf tip, all indicative of a developmentally tuned regulation of SE diameter and forisome size. Heat-induced forisome dispersion occurred later with increasing distance from the stimulus site. T. pratense and V. faba dispersion occurred faster for forisomes with a smaller surface area. Near the stimulus site, electro potential waves (EPWs)-overlapping action (APs), and variation potentials (VPs)-were linked with high full-dispersion rates of forisomes. Distance-associated reduction of forisome reactivity was assigned to the disintegration of EPWs into APs, VPs and system potentials (SPs). Overall, APs and SPs alone were unable to induce forisome dispersion and only VPs above a critical threshold were capable of inducing forisome reactions.

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The plant primary energy metabolism is profoundly reorganized under biotic stress conditions and there is increasing evidence for a role of the fermentative pathway in biotic interactions. Previously we showed via transient gene silencing or overexpression a function of barley alcohol dehydrogenase 1 (HvADH-1) in the interaction of barley with the parasitic fungus Blumeria graminis f.sp. hordei (Bgh). Here we extend our studies on stable transgenic barley events over- or under-expressing HvADH-1 to analyse ADH-1 functions at the level of whole plants. Knock-down (KD) of HvADH-1 by dsRNA interference resulted in reduced and overexpression of HvADH-1 in strongly increased HvADH-1 enzyme activity in leaves of stable transgenic barley plants. The KD of HvADH-1 coincided with a reduced susceptibility to Bgh of both excised leaves and leaves of intact plants. Overexpression (OE) of HvADH-1 results in increased susceptibility to Bgh when excised leaves but not when whole seedlings were inoculated. When first leaves of 10-day-old barley plants were treated with a chitin elicitor, we observed a reduced enzyme activity of ADH-1/-1 homodimers at 48 h after treatment in the second, systemic leaf for empty vector controls and HvADH-1 KD events, but not for the HvADH-1 OE events. Reduced ADH-1 activity in the systemic leaf of empty vector controls and HvADH-1 KD events coincided with chitin-induced resistance to Bgh. Taken together, stable HvADH-1 (KD) or systemic down-regulation of ADH-1/-1 activity by chitin treatment modulated the pathogen response of barley to the biotrophic fungal parasite Bgh and resulted in less successful infections by Bgh.

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Long-distance signalling is important for coordinating plant responses to the environment. Variation potentials (VPs) are a type of long-distance electrical signal that are generated in plants in response to wounding or flaming. Unlike self-propagating action potentials, VPs can be measured beyond regions of dead or chemically treated tissue that block signal generation, suggesting a different mode of propagation. Two alternative propagation mechanisms have been proposed: movement of a chemical agent and a pressure wave through the vasculature. Variants of these two signalling mechanisms have been suggested. Here, we use simple models of the underlying physical processes to evaluate and compare these predictions against independent data. Our models suggest that chemical diffusion and pressure waves are unlikely to capture existing data with parameters that are known from other sources. The previously discarded hypothesis of mass flow in the xylem transporting a chemical agent, however, is able to reproduce experimental propagation speeds for VPs. We therefore suggest that chemical agents transported by mass flow within the xylem are more likely than a pressure wave or chemical diffusion as a VP propagation mechanism. Understanding this mode of long-distance signalling within plants is important for unravelling how plants coordinate physiological responses via cell-to-cell communication.

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Rapid long-distance signalling is an emerging topic in plant research, and is particularly associated with responses to biotic and abiotic stress. Systemic acquired resistance (SAR) to pathogen attack is dependent on nitric oxide (NO) and reactive oxygen species (ROS) such as hydrogen peroxide (H2 O2 ). By comparison, systemic wound responses (SWRs) and systemic acquired acclimation (SAA) to abiotic stress encounters are triggered by rapid waves of H2 O2 , calcium and electrical signalling. Efforts have been made to decipher the relationship between redox messengers, calcium and other known systemic defence signals. Less is known about possible routes of signal transduction throughout the entire plant. Previously, the phloem has been suggested to be a transport conduit for mobile signals inducing SAR, SWR and SAA. This review highlights the role of the phloem in systemic redox signalling by NO and ROS. A not yet identified calcium-dependent NO source and S-nitrosoglutathione reductase are candidate regulators of NO homeostasis in the phloem, whereas ROS concentrations are controlled by NADPH oxidases and the H2 O2 -scavenging enzyme ascorbate peroxidase. Possible amplification mechanisms in phloem-mediated systemic redox signalling are discussed.

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Strigolactones (SL) contribute to drought acclimatization in shoots, because SL-depleted plants are hypersensitive to drought due to stomatal hyposensitivity to abscisic acid (ABA). However, under drought, SL biosynthesis is repressed in roots, suggesting organ specificity in their metabolism and role. Because SL can be transported acropetally, such a drop may also affect shoots, as a systemic indication of stress. We investigated this hypothesis by analysing molecularly and physiologically wild-type (WT) tomato (Solanum lycopersicum) scions grafted onto SL-depleted rootstocks, compared with self-grafted WT and SL-depleted genotypes, during a drought time-course. Shoots receiving few SL from the roots behaved as if under mild stress even if irrigated. Their stomata were hypersensitive to ABA (likely via a localized enhancement of SL synthesis in shoots). Exogenous SL also enhanced stomata sensitivity to ABA. As the partial shift of SL synthesis from roots to shoots mimics what happens under drought, a reduction of root-produced SL might represent a systemic signal unlinked from shootward ABA translocation, and sufficient to prime the plant for better stress avoidance.

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Calcium ion (Ca(2+) ) signalling triggered by insect herbivory is an intricate network with multiple components, involving positive and negative regulators. Real-time, noninvasive imaging of entire Arabidopsis thaliana rosettes was employed to monitor cytosolic free calcium ([Ca(2+) ]cyt ) elevations in local and systemic leaves in response to wounding and Spodoptera littoralis feeding. Luminescence emitted by the cytosol-localized Ca(2+) reporter aequorin was imaged using a high-resolution photon-counting camera system. Spodoptera littoralis feeding on Arabidopsis induced both local and systemic [Ca(2+) ]cyt elevations. Systemic [Ca(2+) ]cyt signals were found predominantly in adjacent leaves with direct vascular connections to the treated leaf and appeared with a delay of 1 to 2 min. Simulated herbivory by wounding always induced a local [Ca(2+) ]cyt response, but a systemic one only when the midrib was wounded. This systemic [Ca(2+) ]cyt response was suppressed by the presence of insect-derived oral secretions as well as in a mutant of the vacuolar cation channel, Two Pore Channel 1 (TPC1). Our results provide evidence that in Arabidopsis insect herbivory induces both local and systemic [Ca(2+) ]cyt signals that distribute within the vascular system. The systemic [Ca(2+) ]cyt signal could play an important signalling role in systemic plant defence.

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The induction and secretion of acid phosphatases (APases) is a universal response of plants to phosphate (Pi) starvation. AtPAP10 (Arabidopsis purple acid phosphatase 10) is a major Pi starvation-induced APase that is associated with the root surface in Arabidopsis. So far, the roles of local and systemic signalling in regulating root-associated AtPAP10 activity remain largely unknown. In this work, we show that a decrease of local, external Pi availability is sufficient to induce AtPAP10 transcription in roots in the presence of sucrose, a systemic signal from shoots, whereas the magnitude of the induction is affected by the Pi status of the whole plant. Once the AtPAP10 mRNAs are synthesized in roots, subsequent accumulation of AtPAP10 proteins in root cells and increase in AtPAP10 activity on the root surface are mainly controlled by local signalling. Previously, ethylene has been demonstrated to be a positive regulator of AtPAP10 activity. In this study, we provide evidence that under Pi deficiency ethylene mainly modulates enzymatic activity of AtPAP10 on the root surface, but not AtPAP10 transcription and protein accumulation, suggesting that it functions as a local signal. Furthermore, our work indicates that the effect of ethylene on the induction of root-associated AtPAP10 activity depends on sucrose, but that the effect of sucrose does not depend on ethylene. These results reveal new insights into the distinct roles of local and systemic signalling in the regulation of root-associated AtPAP10 activity under Pi starvation.

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The ability of plants to sense their nitrogen (N) microenvironment in the soil and deploy strategic root growth in N-rich patches requires exquisite systems integration. Remarkably, this new paradigm for systems biology research has intrigued plant biologists for more than a century, when a split-root framework was first used to study how plants sense and respond to heterogeneous soil nutrient environments. This systemic N-signalling mechanism, allowing plants to sense and forage for mineral nutrients in resource-rich patches, has important implications for agriculture. In this review, we will focus on how advances in the post-genomic era have uncovered the gene regulatory networks underlying systemic N-signalling. After defining how local and systemic N-signalling can be experimentally distinguished for molecular study using a split-root system, the genetic factors that have been shown to mediate local and/or systemic N-signalling are reviewed. Second, the genetic mechanism of this regulatory system is broadened to the whole genome level. To do this, publicly available N-related transcriptomic datasets are compared with genes that have previously been identified as local and systemic N responders in a split-root transcriptome dataset. Specifically, (i) it was found that transcriptional reprogramming triggered by homogeneous N-treatments is composed of both local and systemic responses, (ii) the spatio-temporal signature of local versus systemic responsive genes is defined, and (iii) the conservation of systemic N-signalling between Arabidopsis and Medicago is assessed. Finally, the potential mediators, i.e. metabolites and phytohormones, of the N-related long-distance signals, are discussed.

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Root growth and development are of outstanding importance for the plant's ability to acquire water and nutrients from different soil horizons. To cope with fluctuating nutrient availabilities, plants integrate systemic signals pertaining to their nutritional status into developmental pathways that regulate the spatial arrangement of roots. Changes in the plant nutritional status and external nutrient supply modulate root system architecture (RSA) over time and determine the degree of root plasticity which is based on variations in the number, extension, placement, and growth direction of individual components of the root system. Roots also sense the local availability of some nutrients, thereby leading to nutrient-specific modifications in RSA, that result from the integration of systemic and local signals into the root developmental programme at specific steps. An in silico analysis of nutrient-responsive genes involved in root development showed that the majority of these specifically responded to the deficiency of individual nutrients while a minority responded to more than one nutrient deficiency. Such an analysis provides an interesting starting point for the identification of the molecular players underlying the sensing and transduction of the nutrient signals that mediate changes in the development and architecture of root systems.

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The objectives of this work using Phaseolus vulgaris were to examine whether the light spectrum incident on mature primary leaves (PLs) is related to leaf-to-leaf systemic regulation of developing trifoliate leaves (TLs) in photosynthetic characteristics, and to investigate the relative importance of spectrum and photosynthetic photon flux density (PPFD) in light-induced systemic regulation. Systemic regulation was induced by altering PPFD and the spectrum of light incident on PLs using a shading treatment and lighting treatments including either white, blue, green or red light-emitting diodes (LEDs). Photosynthetic characteristics were evaluated by measuring the light-limited and light-saturated net photosynthetic rates and the amounts of nitrogen (N), chlorophyll (Chl) and ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco; EC 4.1.1.39). Shading treatment on PLs decreased the amounts of N, Chl and Rubisco of TLs and tended to decrease the photosynthetic rates. However, we observed no systemic effects induced by the light spectrum on PLs in this study, except that a higher amount of Rubisco of TLs was observed when the PLs were irradiated with blue LEDs. Our results imply that photoreceptors in mature leaves have little influence on photosynthetic rates and amounts of N and Chl of developing leaves through systemic regulation, although the possibility of the action of blue light irradiation on the amount of Rubisco cannot be ruled out. Based on these results, we concluded that the light spectrum incident on mature leaves has little systemic effect on developing leaves in terms of photosynthetic characteristics and that the light-induced systemic regulation was largely accounted for by PPFD.

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