MYB30 Orchestrates Systemic Reactive Oxygen Signaling and Plant Acclimation

Abstract

Systemic acquired acclimation (SAA) is a key biological process essential for plant survival under conditions of abiotic stress. SAA was recently shown to be controlled by a rapid systemic signaling mechanism termed the reactive oxygen species (ROS) wave in Arabidopsis (Arabidopsis thaliana). MYB30 is a key transcriptional regulator mediating many different biological processes. MYB30 was found to act downstream of the ROS wave in systemic tissues of Arabidopsis in response to local high light (HL) stress treatment. However, the function of MYB30 in systemic signaling and SAA is unknown. To determine the relationship among MYB30, the ROS wave, and systemic acclimation in Arabidopsis, the SAA response to HL stress of myb30 mutants and wild-type plants was determined. Although myb30 plants were found to display enhanced rates of ROS wave propagation and their local tissues acclimated to the HL stress, they were deficient in SAA to HL stress. Compared to wild type, the systemic transcriptomic response of myb30 plants was also deficient, lacking in the expression of over 3,500 transcripts. A putative set of 150 core transcripts directly associated with MYB30 function during HL stress was determined. Our study identifies MYB30 as a key regulator that links systemic ROS signaling with systemic transcriptomic responses, SAA, and plant acclimation to HL stress. In addition, it demonstrates that plant acclimation and systemic ROS signaling are interlinked and that the lack of systemic acclimation drives systemic ROS signaling to occur at faster rates, suggesting a feedback mechanism (potentially involving MYB30) between these two processes.

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

“…3A). Analysis of transcript expression in local and systemic tissues of these mutants, in response to a local HL stress treatment, revealed that the steady-state level of different acclimation transcripts such as ZAT10 and ZAT12 ( 6, 9, 20, 21 ) was enhanced in local leaves (that were directly subjected to the HL treatment) of all mutants. With the exception of glr3.3glr3.6 , that displayed suppressed expression of acclimation transcripts in systemic leaves, the expression of ZAT10 and ZAT12 in systemic tissues of all other mutants was repressed (Fig.…”

“…( B ) Real-time quantitative PCR analysis of transcript expression in local and systemic leaves of wild-type and the glr3.3glr3.6, cngc2, msl2,pip2;1 and pdlp5 mutants subjected to a local 0, 2 or 10 min HL treatment. Transcripts tested ( ZAT12, ZAT10, MYB30 ) were previously found to respond to HL stress at the local and systemic leaves of wild-type plants ( 6, 9, 20, 21 ). Results, expressed in RQ (relative quantity), were obtained by normalizing relative transcript expression and comparing it to control wild type from local leaf.…”

“…Systemic ROS signals could therefore be controlled by multiple different pathways, some promoting them and some suppressing or altering their signature ( 3, 4, 8, 24 ). Supporting the existence of ROS wave-suppressing pathways is a recent study showing that the transcription factor MYB30 regulates a pathway that suppresses systemic ROS signals in response to excess light stress ( 21 ).…”

“…Quantified total RNA was used for cDNA synthesis (PrimeScript RT Reagent Kit, Takara Bio, Kusatsu, Japan). Transcript expression was quantified by real-time qPCR using iQ SYBR Green supermix (Bio-Rad Laboratories, Hercules, CA, USA), as described in ( 6, 9, 14, 18, 21 ), with specific primers for: ZAT12 (AT5G59820) 5’-TGGGAAGAGAGTGGCTTGTTT-3’ and 5’-TAAACTGTTCTTCCAAGCTCCA-3’, ZAT10 (AT1G27730) 5’-ACTAGCCACG TTAGCAGTAGC-3’ and 5’-GTTGAAGTTTGACCGGAAGTC-3’, and MYB30 (AT3G28910) 5’-CCACTTGGCGAAAAAGGCTC-3’ and 5’-ACCCGCTAGCTGAGGAAGTA-3’ Elongation factor 1 alpha (5’-GAGCCCAAGTTTTTGAAGA-3’ and 5’-TAAACTGTTCTTCCAAGCTCCA-3’) was used for normalization of relative transcript levels. Results, expressed in RQ (relative quantity) were obtained by normalizing relative transcript expression and comparing it to control wild type from local leaf.…”

“…Among the many different systemic signaling pathways thought to mediate rapid systemic responses and SAA or SWR are electrical, calcium, hydraulic, and ROS waves ( 6–8, 10, 12, 13, 21–23 ). Electrical signals and calcium waves were recently shown to be dependent on the function of the calcium-permeable glutamate receptor-like (GLR) GLR3.3 and GLR3.6 channels during SWR ( 7, 10, 13, 23 ), and calcium and ROS waves were proposed to be linked through the function of the respiratory burst oxidase homolog D (RBOHD) protein during systemic responses to light and salt stress ( 6, 15, 17, 24, 25 ).…”