Vascular Bundles Mediate Systemic Reactive Oxygen Signaling during Light Stress

Abstract

Short title: Vascular bundles mediate systemic ROS signaling One sentence summary: The reactive oxygen species wave propagates through vascular bundles during the systemic response of Arabidopsis thaliana plants to excess light stress.

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

“…In addition to activating acclimation mechanisms at the specific plant tissue(s) exposed to stress, different abiotic stresses, as well as mechanical injury, can trigger rapid systemic signaling pathways that result in systemic acquired acclimation (SAA), or systemic wound responses (SWR), at the whole-plant level ( 5–18 ). In the case of abiotic stresses, such as excess light or heat stresses, the process of rapid systemic signaling and SAA result in the protection of plants from a subsequent exposure to abiotic stress ( 9, 14, 19–22 ).…”

“…Activation of RBOHD results in the generation of superoxide (O 2 − ) molecules that dismutate into hydrogen peroxide (H 2 O 2 ) at the apoplast, and aquaporins such as plasma membrane (PM) intrinsic protein channels (PIPs, 31, 32 ) were demonstrated to regulate H 2 O 2 translocation across the PM from the apoplast into the cytosol. The translocation of H 2 O 2 into the cytosol enables it to alter different redox-dependent reactions, kinases/phosphatase molecular switches, and/or calcium-permeable channels, further driving different local and systemic acclimation pathways ( 6, 8, 9, 19–22, 25, 31 ). This type of apoplast-to-cytosol translocation of signaling molecules such as H 2 O 2 is also responsible for cell-to-cell communication of systemic signals during SAA ( 6, 8, 9, 18–22 ).…”

“…The translocation of H 2 O 2 into the cytosol enables it to alter different redox-dependent reactions, kinases/phosphatase molecular switches, and/or calcium-permeable channels, further driving different local and systemic acclimation pathways ( 6, 8, 9, 19–22, 25, 31 ). This type of apoplast-to-cytosol translocation of signaling molecules such as H 2 O 2 is also responsible for cell-to-cell communication of systemic signals during SAA ( 6, 8, 9, 18–22 ). A signaling compound such as H 2 O 2 , produced by one cell could therefore enter a neighboring cell and trigger acclimation and defense mechanisms in it, resulting in the activation of its own RBOHD, and a chain of cell-to-cell transmission of this type of signal ( i.e ., the ROS wave) could mediate rapid systemic signaling ( 6, 8, 14, 19–22, 33–35 ).…”

“…This type of apoplast-to-cytosol translocation of signaling molecules such as H 2 O 2 is also responsible for cell-to-cell communication of systemic signals during SAA ( 6, 8, 9, 18–22 ). A signaling compound such as H 2 O 2 , produced by one cell could therefore enter a neighboring cell and trigger acclimation and defense mechanisms in it, resulting in the activation of its own RBOHD, and a chain of cell-to-cell transmission of this type of signal ( i.e ., the ROS wave) could mediate rapid systemic signaling ( 6, 8, 14, 19–22, 33–35 ). In addition to such an apoplastic route of H 2 O 2 –to-cytosol translocation among different cells during systemic signaling, a symplastic plasmodesmata (PD)-dependent route of systemic signaling could also be playing a role in the translocation of systemic signals, mediating different calcium, redox or kinases/phosphatase switch modes between cells ( 7, 17, 36–38 ).…”

“…In addition, although PD pore size was proposed to be regulated by changes in redox levels ( 42–45 ), whether or not PD transport is regulated by ROS during rapid systemic signaling and SAA to excess light stress is currently unknown. Here, using a newly developed method to image ROS signals in live plants grown in soil ( 8, 20–22, 46 ), coupled with different grafting and acclimation studies, we studied the regulation of systemic signals in wild type and many different Arabidopsis thaliana mutants impaired in ROS, calcium, PD and aquaporin functions (table S1) in response to a local application of light stress.…”