Nucleoredoxin2 (NRX2) Promotes Jasmonate-Mediated Trichome Formation in Arabidopsis

다국어 초록 (Multilingual Abstract)

Thioredoxin (Trx) proteins are essential for the maintenance of cellular redox balance through thiol/disulfide exchange modification. In Arabidopsis, the Trx superfamily consists of multiple protein isotypes distributed in most cellular compartments. Although the functions of chloroplastic and cytosolic Trxs have been investigated in plants, the physiological role of nuclear Trx proteins remains elusive. Nucleoredoxin (NRX) is a nuclear Trx first identified in eukaryotic organisms. Arabidopsis possesses two NRX genes (AtNRX1 and AtNRX2), and the function of AtNRX2 has not been elucidated to date. In this study, we characterized the function of AtNRX2 using the atnrx2 knockout mutant, based on its comparison with the atnrx1 mutant. In atnrx2 knockout mutant plants, trichome number was significantly reduced compared with the wild type (WT; Col-0) and the atnrx1 mutant. In response to JA induction of trichome, trichome formation was markedly diminished in the atnrx2 mutant. In addition, expression levels of genes involved in trichome formation were reduced in the atnrx2 mutant compared with the WT and atnrx1 mutant. Overall, our results suggest that AtNRX2 plays a physiological role in JA-mediated trichome formation in Arabidopsis.

참고문헌 (Reference)

1 Naranjo B, "Type-f thioredoxins have a role in the short-term activation of carbon metabolism and their loss affects growth under short-day conditions in Arabidopsis thaliana" 67 : 1951-1964, 2016

2 Jang HH, "Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function" 117 : 625-635, 2004

3 Lemaire SD, "Thioredoxins in chloroplasts" 51 : 343-365, 2007

4 Meyer Y, "Thioredoxins and glutaredoxins : unifying elements in redox biology" 43 : 335-367, 2009

5 Holmgren A, "Thioredoxin" 54 : 237-271, 1985

6 Funato Y, "The thioredoxinrelated redox-regulating protein nucleoredoxin inhibits Wnt-betacatenin signalling through dishevelled" 8 : 501-508, 2006

7 Fambrini M, "The dynamic genetic-hormonal regulatory network controlling the trichome development in leaves" 8 : 253-, 2019

8 Roos G, "The conserved active site proline determines the reducing power of Staphylococcus aureus thioredoxin" 368 : 800-811, 2007

9 Zhao M, "The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci" 135 : 1991-1999, 2008

10 Walker AR, "The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein" 11 : 1337-1350, 1999

11 Qi T, "The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonatemediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana" 23 : 1795-1814, 2011

12 Pesch M, "TRANSPARENT TESTA GLABRA1 and GLABRA1 compete for binding to GLABRA3 in Arabidopsis" 168 : 584-597, 2015

13 Larkin JC, "Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA genes in Arabidopsis trichome development" 6 : 1065-1076, 1994

14 Funato Y, "Redox regulation of Wnt signalling via nucleoredoxin" 44 : 379-388, 2010

15 Szymanski DB, "Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis" 5 : 214-219, 2000

16 Asada K, "Production and scavenging of reactive oxygen species in chloroplasts and their functions" 141 : 391-396, 2006

17 Arsova B, "Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner : evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana" 22 : 1498-1515, 2010

18 Vieira Dos Santos C, "Plant thioredoxins are key actors in the oxidative stress response" 11 : 329-334, 2006

19 Tada Y, "Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins" 321 : 952-956, 2008

20 Qin Y, "Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil" 5 : e1000621-, 2009

21 Hirota K, "Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells" 274 : 177-182, 2000

22 Funato Y, "Nucleoredoxin, a novel thioredoxin family member involved in cell growth and differentiation" 9 : 1035-1057, 2007

23 Hayashi T, "Nucleoredoxin negatively regulates Toll-like receptor 4 signaling via recruitment of flightless-I to myeloid differentiation primary response gene(88)" 285 : 18586-18593, 2010

24 Wagner GJ, "New approaches for studying and exploiting an old protuberance, the plant trichome" 93 : 3-11, 2004

25 Marchal C, "NTR/NRX define a new thioredoxin system in the nucleus of Arabidopsis thaliana cells" 7 : 30-44, 2014

26 Yoshida Y, "Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis" 136 : 1039-1048, 2009

27 Traw MB, "Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis" 133 : 1367-1375, 2003

28 Gan Y, "Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8and GIS2 in the regulation of epidermal cell fate" 134 : 2073-2081, 2007

29 Laloi C, "Identification and characterization of a mitochondrial thioredoxin system in plants" 98 : 14144-14149, 2001

30 Lawrence T, "IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation" 434 : 1138-1143, 2005

31 Park SK, "Heat-shock and redoxdependent functional switching of an h-type Arabidopsis thioredoxin from a disulfide reductase to a molecular chaperone" 150 : 552-561, 2009

32 Payne CT, "GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1" 156 : 1349-1362, 2000

33 Mauricio R, "Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense" 51 : 1435-1444, 1997

34 Wada T, "Epidermal cell differentiation in Arabidopsis determined by a Myb Homolog, CPC" 277 : 1113-1116, 1997

35 Yan C, "Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor" 17 : 7416-7429, 1998

36 Xue LJ, "Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus" 25 : 2714-2730, 2013

37 Kurooka H, "Cloning and characterization of the nucleoredoxin gene that encodes a novel nuclear protein related to thioredoxin" 39 : 331-339, 1997

38 Chibani K, "Atypical thioredoxins in poplar : the glutathione-dependent thioredoxin-like 2. 1 supports the activity of target enzymes possessing a single redox active cysteine" 159 : 592-605, 2012

39 Serrato AJ, "AtCXXS : atypical members of the Arabidopsis thaliana thioredoxin h family with a remarkably high disulfide isomerase activity" 133 : 611-622, 2008

40 Muller L, "An interaction between human Sec63 and nucleoredoxin may provide the missing link between the SEC63 gene and polycystic liver disease" 585 : 596-600, 2011

41 Delaunay A, "A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation" 111 : 471-481, 2002

42 Morohashi K, "A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors" 5 : e1000396-, 2009

43 Gelhaye E, "A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase" 101 : 14545-14550, 2004

44 Laughner BJ, "A novel nuclear member of the thioredoxin superfamily" 118 : 987-996, 1998

45 Oppenheimer DG, "A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules" 67 : 483-493, 1991