Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis

Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (the local tissue) to the entire plant (systemic tissues). Reactive oxygen species (ROS) and Ca2+ are key signaling molecules thought to be involved in this cell-to-cell mechanism. Here, we report that the systemic response of Arabidopsis thaliana to a local treatment of high light stress, which resulted in local ROS accumulation, required ROS generated by respiratory burst oxidase homolog D (RBOHD). ROS increased cell-to-cell transport and plasmodesmata (PD) pore size in a manner dependent on PD-localized protein 1 (PDLP1) and PDLP5, and this process was required for the propagation of the systemic ROS signals and SAA. Furthermore, aquaporins and several Ca2+-permeable channels in the glutamate receptor–like (GLR), mechanosensitive small conductance–like (MSL), and cyclic nucleotide–gated (CNGC) families were involved in this systemic signaling process. However, we determined that these channels were required primarily to amplify the systemic signal in each cell along the path of the systemic ROS wave, as well as to establish local and systemic acclimation. Thus, PD and RBOHD-generated ROS orchestrate light stress–induced rapid cell-to-cell spread of systemic signals in Arabidopsis.

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Plasmodesmata-localized proteins and reactive oxygen species orchestrate light-induced rapid systemic signaling in Arabidopsis

10.1101/2020.10.07.329995 ◽

2020 ◽

Author(s):

Yosef Fichman ◽

Ronald J. Myers ◽

DeAna G. Grant ◽

Ron Mittler

Keyword(s):

Reactive Oxygen Species ◽

Light Stress ◽

Reactive Oxygen ◽

Oxygen Species ◽

Cell Transport ◽

Systemic Signaling ◽

Entire Plant ◽

Systemic Signal ◽

Respiratory Burst Oxidase ◽

Systemic Signals

AbstractSystemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (local tissue) to the entire plant (systemic tissues). Among the different systemic signaling molecules and processes thought to be involved in this cell-to-cell signaling mechanism are reactive oxygen species (ROS), calcium, electric and hydraulic signals. How these different signals and processes are interlinked, and how they transmit the systemic signal all the way from the local tissue to the entire plant, remain however largely unknown. Here, studying the systemic response of Arabidopsis thaliana to a local treatment of excess light stress, we report that respiratory burst oxidase homolog D (RBOHD)-generated ROS enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of systemic signals during responses to light stress. We further identify aquaporins, and several different calcium-permeable channels, belonging to the glutamate receptor-like, mechanosensitive small conductance-like, and cyclic nucleotide-gated families, as involved in this process, but determine that their function is primarily required for the maintenance of the signal in each cell along the path of the systemic signal, as well as for the establishment of acclimation at the local and systemic tissues. PD and RBOHD-generated ROS orchestrate therefore light stress-induced rapid cell-to-cell spread of systemic signals in Arabidopsis.One-sentence summaryRespiratory burst oxidase homolog D-generated reactive oxygen species enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of the PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of rapid systemic signals during the response of Arabidopsis to excess light stress.

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FMO1 Is Involved in Excess Light Stress-Induced Signal Transduction and Cell Death Signaling

Cells ◽

10.3390/cells9102163 ◽

2020 ◽

Vol 9 (10) ◽

pp. 2163 ◽

Cited By ~ 1

Author(s):

Weronika Czarnocka ◽

Yosef Fichman ◽

Maciej Bernacki ◽

Elżbieta Różańska ◽

Izabela Sańko-Sawczenko ◽

...

Keyword(s):

Cell Death ◽

Signaling Pathways ◽

Systemic Acquired Resistance ◽

Light Stress ◽

Acquired Resistance ◽

Defense Responses ◽

Cellular Mechanisms ◽

Systemic Signal ◽

Excess Light ◽

Induced Signal

Because of their sessile nature, plants evolved integrated defense and acclimation mechanisms to simultaneously cope with adverse biotic and abiotic conditions. Among these are systemic acquired resistance (SAR) and systemic acquired acclimation (SAA). Growing evidence suggests that SAR and SAA activate similar cellular mechanisms and employ common signaling pathways for the induction of acclimatory and defense responses. It is therefore possible to consider these processes together, rather than separately, as a common systemic acquired acclimation and resistance (SAAR) mechanism. Arabidopsis thaliana flavin-dependent monooxygenase 1 (FMO1) was previously described as a regulator of plant resistance in response to pathogens as an important component of SAR. In the current study, we investigated its role in SAA, induced by a partial exposure of Arabidopsis rosette to local excess light stress. We demonstrate here that FMO1 expression is induced in leaves directly exposed to excess light stress as well as in systemic leaves remaining in low light. We also show that FMO1 is required for the systemic induction of ASCORBATE PEROXIDASE 2 (APX2) and ZINC-FINGER OF ARABIDOPSIS 10 (ZAT10) expression and spread of the reactive oxygen species (ROS) systemic signal in response to a local application of excess light treatment. Additionally, our results demonstrate that FMO1 is involved in the regulation of excess light-triggered systemic cell death, which is under control of LESION SIMULATING DISEASE 1 (LSD1). Our study indicates therefore that FMO1 plays an important role in triggering SAA response, supporting the hypothesis that SAA and SAR are tightly connected and use the same signaling pathways.

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Hydrogen peroxide plays an important role in PERK4-mediated abscisic acid-regulated root growth in Arabidopsis

Functional Plant Biology ◽

10.1071/fp18219 ◽

2019 ◽

Vol 46 (2) ◽

pp. 165 ◽

Cited By ~ 15

Author(s):

Xiaonan Ma ◽

Xiaoran Zhang ◽

Ling Yang ◽

Mengmeng Tang ◽

Kai Wang ◽

...

Keyword(s):

Hydrogen Peroxide ◽

Abscisic Acid ◽

Root Growth ◽

Primary Root ◽

Root Tip ◽

Exogenous Aba ◽

Ros Accumulation ◽

Primary Root Growth ◽

Respiratory Burst Oxidase ◽

Respiratory Burst Oxidase Homologue

Abscisic acid (ABA) is a crucial factor that affects primary root tip growth in plants. Previous research suggests that reactive oxygen species (ROS), especially hydrogen peroxide, are important regulators of ABA signalling in root growth of Arabidopsis. PROLINE-RICH EXTENSIN-LIKE RECEPTOR KINASE 4 (PERK4) plays an important role in ABA responses. Arabidopsis perk4 mutants display attenuated sensitivity to ABA, especially in primary root growth. To gain insights into the mechanism(s) of PERK4-associated ABA inhibition of root growth, in this study we investigated the involvement of ROS in this process. Normal ROS accumulation in the primary root in response to exogenous ABA treatment was not observed in perk4 mutants. PERK4 deficiency prohibits ABA-induced expression of RESPIRATORY BURST OXIDASE HOMOLOGUE (RBOH) genes, therefore the perk4-1 mutant showed decreased production of ROS in the root. The perk4-1/rbohc double mutant displayed the same phenotype as the perk4 and rbohc single mutants in response to exogenous ABA treatment. The results suggest that PERK4-stimulated ROS accumulation during ABA-regulated primary root growth may be mediated by RBOHC.

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The host jasmonic acid pathway regulates the transcriptomic changes of dodder and host plant under the scenario of caterpillar feeding on dodder

BMC Plant Biology ◽

10.1186/s12870-019-2161-8 ◽

2019 ◽

Vol 19 (1) ◽

Author(s):

Yan Qin ◽

Jingxiong Zhang ◽

Christian Hettenhausen ◽

Hui Liu ◽

Shalan Li ◽

...

Keyword(s):

Jasmonic Acid ◽

Host Plant ◽

Host Plants ◽

Systemic Signaling ◽

Lepidopteran Insects ◽

Acid Pathway ◽

Plant Translocation ◽

Transcriptomic Changes ◽

Systemic Responses ◽

Systemic Signals

Abstract Background Dodder (Cuscuta spp., Convolvulaceae) species are obligate leaf- and rootless parasites that totally depend on hosts to survive. Dodders naturally graft themselves to host stems to form vascular fusion, from which they obtain nutrients and water. In addition, dodders and their hosts also exchange various other molecules, including proteins, mRNAs, and small RNAs. It is very likely that vascular fusion also allows inter-plant translocation of systemic signals between dodders and host plants and these systemic signals may have profound impacts on the physiology of dodder and host plants. Herbivory is a common biotic stress for plants. When a dodder parasite is attacked by lepidopteran insects, how dodder responds to caterpillar feeding and whether there are inter-plant communications between the host plants and the parasites is still poorly understood. Results Here, wild-type (WT) tobacco and a tobacco line in which jasmonic acid (JA) biosynthesis was silenced (AOC-RNAi) were used as the hosts, and the responses of dodders and their host plants to herbivory by Spodoptera litura caterpillars on the dodders were investigated. It was found that after caterpillar attack, dodders grown on AOC-RNAi tobacco showed much a smaller number of differentially expressed genes, although the genotypes of the tobacco plants did not have an effect on the simulated S. litura feeding-induced JA accumulation in dodders. We further show that S. litura herbivory on dodder also led to large changes in transcriptome and defensive metabolites in the host tobacco, leading to enhanced resistance to S. litura, and the JA pathway of tobacco host is critical for these systemic responses. Conclusions Our findings indicate that during caterpillar attack on dodder, the JA pathway of host plant is required for the proper transcriptomic responses of both dodder and host plants. This study highlights the importance of the host JA pathway in regulating the inter-plant systemic signaling between dodder and hosts.

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Untangling the ties that bind different systemic signals in plants

Science Signaling ◽

10.1126/scisignal.abb9505 ◽

2020 ◽

Vol 13 (640) ◽

pp. eabb9505

Author(s):

Yosef Fichman ◽

Sara I. Zandalinas ◽

Ron Mittler

Keyword(s):

Complex Network ◽

Cell Types ◽

Systemic Response ◽

Systemic Signaling ◽

Systemic Signals

Systemic signaling in plants is orchestrated by a complex network of interconnected systemic signals and cell types. In this issue of Science Signaling, Shao et al. unveil how different wound-induced signals integrate into a well-regulated systemic response.

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Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants

10.1101/2021.02.12.430927 ◽

2021 ◽

Author(s):

Yosef Fichman ◽

Ron Mittler

Keyword(s):

Reactive Oxygen Species ◽

Membrane Potential ◽

Reactive Oxygen ◽

Hydraulic Pressure ◽

Oxygen Species ◽

Plant Survival ◽

Systemic Signaling ◽

Entire Plant ◽

Different Types ◽

Systemic Signals

AbstractThe sensing of abiotic stress, mechanical injury, or pathogen attack by a single plant tissue results in the activation of systemic signals that travel from the affected tissue to the entire plant, alerting it of an impending stress or pathogen attack. This process is essential for plant survival during stress and is termed systemic signaling. Among the different signals triggered during this process are calcium, electric, reactive oxygen species (ROS) and hydraulic signals. These are thought to propagate at rapid rates through the plant vascular bundles and to regulate many of the systemic processes essential for plant survival. Although the different signals activated during systemic signaling are thought to be interlinked, their coordination and hierarchy remain to be determined. Here, using a combination of advanced whole-plant imaging and hydraulic pressure measurements, we studied the activation of all four systemic signals in wild type and different Arabidopsis thaliana mutants subjected to a local high light (HL) stress or wounding. Our findings reveal that in response to wounding systemic changes in membrane potential, calcium, ROS, and hydraulic pressure are coordinated by glutamate receptor-like (GLR) proteins 3.3 and 3.6, while in response to HL the respiratory burst oxidase homolog D-driven systemic ROS signal could be separated from systemic changes in membrane potential and calcium levels. We further determine that plasmodesmata functions are required for systemic changes in membrane potential, calcium, and ROS during systemic signaling. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress.Significance statementThe ability of plants to transmit a signal from a stressed or wounded tissue to the entire plant, termed systemic signaling, is key to plant survival during conditions of environmental stress. At least four different systemic signals are thought to be involved in this process: electric, calcium, reactive oxygen and hydraulic. However, how are they coordinated and whether they can be stress-specific is mostly unknown. Here we report that different types of stimuli can induce different types of systemic signals that may or may not be linked with each other. We further reveal that hydraulic waves can be actively regulated in plants in response to wounding, and that proteins that regulate plasmodesmata pores play a key role in systemic signaling.

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Systemic signaling during abiotic stress combination in plants

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2005077117 ◽

2020 ◽

Vol 117 (24) ◽

pp. 13810-13820 ◽

Cited By ~ 13

Author(s):

Sara I. Zandalinas ◽

Yosef Fichman ◽

Amith R. Devireddy ◽

Soham Sengupta ◽

Rajeev K. Azad ◽

...

Keyword(s):

Abiotic Stress ◽

Abiotic Stresses ◽

Systemic Response ◽

Single Leaf ◽

Systemic Signaling ◽

Whole Plant ◽

Significant Difference ◽

Plant Acclimation ◽

Shed Light ◽

Systemic Signals

Extreme environmental conditions, such as heat, salinity, and decreased water availability, can have a devastating impact on plant growth and productivity, potentially resulting in the collapse of entire ecosystems. Stress-induced systemic signaling and systemic acquired acclimation play canonical roles in plant survival during episodes of environmental stress. Recent studies revealed that in response to a single abiotic stress, applied to a single leaf, plants mount a comprehensive stress-specific systemic response that includes the accumulation of many different stress-specific transcripts and metabolites, as well as a coordinated stress-specific whole-plant stomatal response. However, in nature plants are routinely subjected to a combination of two or more different abiotic stresses, each potentially triggering its own stress-specific systemic response, highlighting a new fundamental question in plant biology: are plants capable of integrating two different systemic signals simultaneously generated during conditions of stress combination? Here we show that plants can integrate two different systemic signals simultaneously generated during stress combination, and that the manner in which plants sense the different stresses that trigger these signals (i.e., at the same or different parts of the plant) makes a significant difference in how fast and efficient they induce systemic reactive oxygen species (ROS) signals; transcriptomic, hormonal, and stomatal responses; as well as plant acclimation. Our results shed light on how plants acclimate to their environment and survive a combination of different abiotic stresses. In addition, they highlight a key role for systemic ROS signals in coordinating the response of different leaves to stress.

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Danger-Associated Peptide Regulates Root Immune Responses and Root Growth by Affecting ROS Formation in Arabidopsis

International Journal of Molecular Sciences ◽

10.3390/ijms21134590 ◽

2020 ◽

Vol 21 (13) ◽

pp. 4590 ◽

Cited By ~ 2

Author(s):

Yanping Jing ◽

Nuo Shen ◽

Xiaojiang Zheng ◽

Aigen Fu ◽

Fugeng Zhao ◽

...

Keyword(s):

Immune Responses ◽

Root Growth ◽

Growth Inhibition ◽

Bacterial Pathogen ◽

Root Growth Inhibition ◽

Signaling Crosstalk ◽

Secondary Messenger ◽

Ros Accumulation ◽

Molecular Patterns ◽

Respiratory Burst Oxidase

Plant elicitor peptides (Peps) are damage/danger-associated molecular patterns (DAMPs) that are perceived by a pair of receptor-like kinases, PEPR1 and PEPR2, to enhance innate immunity and induce the growth inhibition of root in Arabidopsis thaliana. In this study, we show that PEPR1 and PEPR2 function vitally in roots to regulate the root immune responses when treating the roots with bacterial pathogen Pst DC3000. PEPR2, rather than PEPR1, played a predominant role in the perception of Pep1 in the roots and further triggered a strong ROS accumulation—the substance acts as an antimicrobial agent or as a secondary messenger in plant cells. Consistently, seedlings mutating two major ROS-generating enzyme genes, respiratory burst oxidase homologs D and F (RBOHD and RBOHF), abolished the root ROS accumulation and impaired the growth inhibition of the roots induced by Pep1. Furthermore, we revealed that botrytis-induced kinase 1 (BIK1) physically interacted with PEPRs and RBOHD/F, respectively, and served downstream of the Pep1-PEPRs signaling pathway to regulate Pep1-induced ROS production and root growth inhibition. In conclusion, this study demonstrates a previously unrecognized signaling crosstalk between Pep1 and ROS signaling to regulate root immune response and root growth.

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