ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling Expression in
Abscisic acid (ABA) plays crucial roles in plant growth and development, and also in plant responses to abiotic and biotic stresses. ABA can stimulate the production of reactive oxygen species (ROS) that act as signals in low concentrations, but as cell-damaging agents in high concentrations. A mutation in ABO8, encoding a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3, leads to hypersensitivity to ABA in root growth, and root tips of the abo8-1 mutants accumulate more ROS than those of the wild type; this accumulation of ROS in abo8-1 root tips is enhanced by ABA treatment. We also found that auxin signaling and/or accumulation is greatly reduced in root tips of the abo8-1 mutants. Addition of the reducing agent GSH to the growth medium partially recovers the root hypersensitivity to ABA, and also the ABA-inhibited expression of PLT1/2 in abo8-1. Furthermore, the inducible expression of PLT2 largely rescues the root growth defect of abo8-1 with and without ABA treatment. Our results reveal the important roles of ROS in regulating root meristem activity in the ABA signaling pathway.
Vyšlo v časopise:
ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling Expression in. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004791
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004791
Souhrn
Abscisic acid (ABA) plays crucial roles in plant growth and development, and also in plant responses to abiotic and biotic stresses. ABA can stimulate the production of reactive oxygen species (ROS) that act as signals in low concentrations, but as cell-damaging agents in high concentrations. A mutation in ABO8, encoding a pentatricopeptide repeat (PPR) protein responsible for the splicing of NAD4 intron 3, leads to hypersensitivity to ABA in root growth, and root tips of the abo8-1 mutants accumulate more ROS than those of the wild type; this accumulation of ROS in abo8-1 root tips is enhanced by ABA treatment. We also found that auxin signaling and/or accumulation is greatly reduced in root tips of the abo8-1 mutants. Addition of the reducing agent GSH to the growth medium partially recovers the root hypersensitivity to ABA, and also the ABA-inhibited expression of PLT1/2 in abo8-1. Furthermore, the inducible expression of PLT2 largely rescues the root growth defect of abo8-1 with and without ABA treatment. Our results reveal the important roles of ROS in regulating root meristem activity in the ABA signaling pathway.
Zdroje
1. De TullioMC, JiangK, FeldmanLJ (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol Biochem 48: 328–336.
2. MittlerR, VanderauweraS, SuzukiN, MillerG, TognettiVB, et al. (2011) ROS signaling: the new wave? Trends Plant Sci 16: 300–309.
3. SuzukiN, KoussevitzkyS, MittlerR, MillerG (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35: 259–270.
4. TognettiVB, MuhlenbockP, Van BreusegemF (2012) Stress homeostasis - the redox and auxin perspective. Plant Cell Environ 35: 321–333.
5. WangP, SongCP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178: 703–718.
6. O'BrienJA, DaudiA, ButtVS, BolwellGP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236: 765–779.
7. De PintoMC, LocatoV, De GaraL (2012) Redox regulation in plant programmed cell death. Plant Cell Environ 35: 234–244.
8. PottersG, PasternakTP, GuisezY, PalmeKJ, JansenMA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12: 98–105.
9. OvermyerK, BroscheM, KangasjarviJ (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8: 335–342.
10. AchardP, RenouJP, BerthomeR, HarberdNP, GenschikP (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18: 656–660.
11. RubinovichL, WeissD (2010) The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. Plant J 64: 1018–1027.
12. Sanchez-FernandezR, FrickerM, CorbenLB, WhiteNS, SheardN, et al. (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci U S A 94: 2745–2750.
13. CobbettCS, MayMJ, HowdenR, RollsB (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. Plant J 16: 73–78.
14. VernouxT, WilsonRC, SeeleyKA, ReichheldJP, MuroyS, et al. (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97–110.
15. YuX, PasternakT, EiblmeierM, DitengouF, KocherspergerP, et al. (2013) Plastid-Localized Glutathione Reductase2-Regulated Glutathione Redox Status Is Essential for Arabidopsis Root Apical Meristem Maintenance. Plant Cell 25: 4451–68.
16. BashandyT, GuilleminotJ, VernouxT, Caparros-RuizD, LjungK, et al. (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22: 376–391.
17. IglesiasMJ, TerrileMC, BartoliCG, D'IppolitoS, CasalongueCA (2010) Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol 74: 215–222.
18. KwakJM, MoriIC, PeiZM, LeonhardtN, TorresMA, et al. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22: 2623–2633.
19. HeJ, DuanY, HuaD, FanG, WangL, et al. (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24: 1815–1833.
20. PencikA, SimonovikB, PeterssonSV, HenykovaE, SimonS, et al. (2013) Regulation of Auxin Homeostasis and Gradients in Arabidopsis Roots through the Formation of the Indole-3-Acetic Acid Catabolite 2-Oxindole-3-Acetic Acid. Plant Cell 25: 3858–70.
21. LiuY, HeJ, ChenZ, RenX, HongX, et al. (2010) ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. Plant J 63: 749–765.
22. BanT, KeJ, ChenR, GuX, TanMH, et al. (2013) Structure of a PLS-Class Pentatricopeptide Repeat Protein Provides Insights into Mechanism of RNA Recognition. J Biol Chem 288: 31540–8.
23. MeyerEH, TomazT, CarrollAJ, EstavilloG, DelannoyE, et al. (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol 151: 603–619.
24. UlmasovT, MurfettJ, HagenG, GuilfoyleTJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963–1971.
25. BenkovaE, MichniewiczM, SauerM, TeichmannT, SeifertovaD, et al. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602.
26. ShibasakiK, UemuraM, TsurumiS, RahmanA (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21: 3823–3838.
27. GalinhaC, HofhuisH, LuijtenM, WillemsenV, BlilouI, et al. (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449: 1053–1057.
28. AidaM, BeisD, HeidstraR, WillemsenV, BlilouI, et al. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109–120.
29. van den BergC, WillemsenV, HageW, WeisbeekP, ScheresB (1995) Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378: 62–65.
30. NakajimaK, BenfeyPN (2002) Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14 Suppl: S265–276.
31. ZhouW, WeiL, XuJ, ZhaiQ, JiangH, et al. (2010) Arabidopsis Tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22: 3692–3709.
32. NakamuraT, YagiY, KobayashiK (2012) Mechanistic insight into pentatricopeptide repeat proteins as sequence-specific RNA-binding proteins for organellar RNAs in plants. Plant Cell Physiol 53: 1171–1179.
33. MillarAH, HeazlewoodJL, KristensenBK, BraunHP, MollerIM (2005) The plant mitochondrial proteome. Trends Plant Sci 10: 36–43.
34. HailiN, ArnalN, QuadradoM, AmiarS, TcherkezG, et al. (2013) The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res 41: 6650–6663.
35. HolzleA, JonietzC, TorjekO, AltmannT, BinderS, et al. (2011) A RESTORER OF FERTILITY-like PPR gene is required for 5′-end processing of the nad4 mRNA in mitochondria of Arabidopsis thaliana. Plant J 65: 737–744.
36. MurayamaM, HayashiS, NishimuraN, IshideM, KobayashiK, et al. (2012) Isolation of Arabidopsis ahg11, a weak ABA hypersensitive mutant defective in nad4 RNA editing. J Exp Bot 63: 5301–5310.
37. SungTY, TsengCC, HsiehMH (2010) The SLO1 PPR protein is required for RNA editing at multiple sites with similar upstream sequences in Arabidopsis mitochondria. Plant J 63: 499–511.
38. TangJ, KobayashiK, SuzukiM, MatsumotoS, MuranakaT (2010) The mitochondrial PPR protein LOVASTATIN INSENSITIVE 1 plays regulatory roles in cytosolic and plastidial isoprenoid biosynthesis through RNA editing. Plant J 61: 456–466.
39. VerbitskiyD, ZehrmannA, van der MerweJA, BrennickeA, TakenakaM (2010) The PPR protein encoded by the LOVASTATIN INSENSITIVE 1 gene is involved in RNA editing at three sites in mitochondria of Arabidopsis thaliana. Plant J 61: 446–455.
40. MohrG, LambowitzAM (2003) Putative proteins related to group II intron reverse transcriptase/maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res 31: 647–652.
41. NakagawaN, SakuraiN (2006) A mutation in At-nMat1a, which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial NAD4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 47: 772–783.
42. KerenI, TalL, des Francs-SmallCC, AraujoWL, ShevtsovS, et al. (2012) nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J 71: 413–426.
43. ZhuQ, DugardeynJ, ZhangC, MuhlenbockP, EastmondPJ, et al. (2013) The Arabidopsis thaliana RNA Editing Factor SLO2, which Affects the Mitochondrial Electron Transport Chain, Participates in Multiple Stress and Hormone Responses. Mol Plant 7: 290–310.
44. YuanH, LiuD (2012) Functional disruption of the pentatricopeptide protein SLG1 affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in Arabidopsis. Plant J 70: 432–444.
45. PeerWA, ChengY, MurphyAS (2013) Evidence of oxidative attenuation of auxin signalling. J Exp Bot 64: 2629–2639.
46. JiangK, MengYL, FeldmanLJ (2003) Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130: 1429–1438.
47. YangXY, ChenZW, XuT, QuZ, PanXD, et al. (2011) Arabidopsis kinesin KP1 specifically interacts with VDAC3, a mitochondrial protein, and regulates respiration during seed germination at low temperature. Plant Cell 23: 1093–1106.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 12
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