Integration of stress-related and reactive oxygen species-mediated signals by Topoisomerase VI in Arabidopsis thaliana

Abstract

Environmental stress often leads to an increased production of reactive oxygen species that are involved in plastid-to-nucleus retrograde signaling. Soon after the release of singlet oxygen ( 1 O 2 ) in chloroplasts of the flu mutant of Arabidopsis , reprogramming of nuclear gene expression reveals a rapid transfer of signals from the plastid to the nucleus. We have identified extraplastidic signaling constituents involved in 1 O 2 -initiated plastid-to-nucleus signaling and nuclear gene activation after mutagenizing a flu line expressing the luciferase reporter gene under the control of the promoter of a 1 O 2 -responsive AAA-ATPase gene ( At3g28580 ) and isolating second-site mutations that lead to a constitutive up-regulation of the reporter gene or abrogate its 1 O 2 -dependent up-regulation. One of these mutants, caa39 , turned out to be a weak mutant allele of the Topoisomerase VI (Topo VI) A-subunit gene with a single amino acid substitution. Transcript profile analysis of flu and flu caa39 mutants revealed that Topo VI is necessary for the full activation of AAA-ATPase and a set of 1 O 2 -responsive transcripts in response to 1 O 2 . Topo VI binds to the promoter of the AAA-ATPase and other 1 O 2 -responsive genes, and hence could directly regulate their expression. Under photoinhibitory stress conditions, which enhance the production of 1 O 2 and H 2 O 2 , Topo VI regulates 1 O 2 -responsive and H 2 O 2 -responsive genes in a distinct manner. These results suggest that Topo VI acts as an integrator of multiple signals generated by reactive oxygen species formed in plants under adverse environmental conditions.

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

“…This pathway may establish a feedback loop for the control of chloroplast ROS level. Topoisomerase VI constitutes another example of an identified cytosolic component that mediates chloroplast 1 O 2 signaling by binding to the promoter of the triple-A ATPase gene, thereby stimulating its expression (Simková et al, 2012). Simultaneously, topoisomerase VI suppresses the expression of H 2 O 2 -stimulated genes.…”

Cellular redox regulation, signaling, and stress response in plants

“…Arabidopsis topoisomerase IV was reported to bind to the promoter of ROS-responsive genes and also integrated 1 O 2 -and H 2 O 2 -responsive genes in a distinct manner. 122) Arabidopsis transcription factors, such as the zinc-finger protein, Zat12, and heat shock factor A2 (HsfA2), which are both highly responsive to ROS irrespective of the kind and source of the compounds, have been identified using comparative transcriptome analysis, which suggests that these transcription factors may be involved in the common pathway. 117) Zat12 and HsfA2 regulate the expression of APX1 and APX2, respectively, through distinct routes, suggesting multiple routes even for the common pathway.…”

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

“…For example, several regulatory molecular components involved in 1 O 2 -mediated plastid-to-nucleus signaling have been identified through extensive genetic mutation screens in the background of the conditional flu mutant, such as EX1, EX2, SOLDAT10, PRL1, CAA33, CAA39 in Arabidopsis. [20][21][22][23][24][25] Two new plastid retrograde signals (PAP and MEcPP) during drought, high light and wounding stress responses have been revealed by two research teams, involving the analysis of the Arabidopsis mutants sal1 and ceh1, which encode the plastid nucleotidase/phosphatase SAL1 and hydroxyl-2-methyl-2-(E)-butenyl4-diphosphate synthase (HDS), respectively. 26,29 Analysis of the rps1 mutant demonstrated that the chloroplast ribosomal protein S1 (RPS1) mediates retrograde signaling to modulate the expression of the heat-responsive nuclear transcription factor HsfA2 and its target genes during heat stress, although the specific plastid retrograde signal is unknown.…”

“…20,21 As an example of the third type, transcript profile analysis of flu and flu caa39 mutants revealed that topoisomerase VI (Topo VI) acts as a nuclear component of 1 O 2 -mediated plastid-to-nucleus signaling to directly regulate the expression of the AAA-ATPase and other 1 O 2 -responsive genes. 25 As an example of the fourth type, mutation of plastid SOLDAT10 disrupts chloroplast homeostasis by attenuating the decrease in plastid-specifc rRNA levels and protein synthesis, and affects the communication of 1 O 2 -mediated signaling between chloroplasts and the nucleus. 22 Similarly, mutation of plastid CAA33 disturbs chloroplast homeostasis by impeding plastid division, interfering with 1 O 2 -mediated plastid-to-nucleus signaling.…”

“…[2][3][4][5][6][7][8][9][10][11][12][13][14][15][16] More recently, several plastid retrograde signaling pathways have been identified to regulate the expression of stress-related nuclear genes during several stresses such as high light, drought, wounding, heat, and excess ammonium. [17][18][19][20][21][22][23][24][25][26][27][28][29][30][31] Based on the new stress-responsive plastid retrograde signaling pathways just reported in 2012 alone, this review will focus on properties of currently proposed molecular components in the plastid retrograde signaling network under stress. We also specifically discuss possible plastid retrograde signals involved in plant response to ammonium stress.…”