Overexpression of the intertidal seagrass J protein ZjDjB1 enhances tolerance to chilling injury

다국어 초록 (Multilingual Abstract)

DnaJ proteins act as molecular chaperones to maintain protein homeostasis under stress. However, their role in seagrass remains largely unidentified. We found that the expression of ZjDjB1, a class II J gene of Zostera japonica, was up-regulated under low-temperature stress. Therefore, we cloned ZjDjB1 from Z. japonica, a typical intertidal seagrass. The role of nuclear and cytoplasmic-targeted DnaJ protein (ZjDjB1) in Z. japonica was studied. Under low-temperature stress, the rates of ger- mination and survival of overexpressed Arabidopsis thaliana were higher than those of the wild-type (WT); the root length was longer; the detached leaves were more tolerant to low temperature, and the chlorophyll content of leaves, relative water content and dry weight of shoot were higher. Overexpressed plants accumulated more osmotic protective substances under low-temperature stress, and the antioxidant enzyme activity of overexpressed plants was higher than that of the WT plants. Under low-temperature stress, overexpressed plants accumulated fewer reactive oxygen species. The root cell viability of overexpressed plants was higher than that of WT under low-temperature stress, and there was minimal membrane damage in the overexpressed plants. Furthermore, the level of expression of CBF1 and CBF target genes, including KIN1 and COR15B, was higher in overexpressed plants than that in the WT plants when subjected to low temperature. These results indicate that ZjDjB1 plays an important role in plant resistance to injury under low-temperature stress.

참고문헌 (Reference)

1 Green R, "UV-B-induced PR-1 accumulation is mediated by active oxygen species" 7 (7): 203-212, 1995

2 Liu QJPC, "Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperatureresponsive gene expression, respectively, in Arabidopsis" 10 (10): 1391-1406, 1998

3 Kreps JA, "Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress" 130 (130): 2129-2141, 2002

4 Short FT, "The seagrass filter: purification of estuarine and coastal waters" Elsevier 1984

5 Craig EA, "The diverse roles of J-proteins, the obligate Hsp70 co-chaperone" 156 : 1-21, 2006

6 Zhang X, "The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis" 212 (212): 345-353, 2016

7 Bukau B, "The Hsp70 and Hsp60 chaperone machines" 92 (92): 351-366, 1998

8 Badawi M, "The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs" 277 (277): 533-554, 2007

9 Bowler C, "Superoxide dismutase and stress tolerance" 43 : 83-116, 1992

10 Michael EC, "Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function" 3 (3): 28-36, 1998

11 Yuan JS, "Statistical analysis of real-time PCR data" 7 : 85-, 2006

12 Eva V, "Signal transduction during oxidative stress" 53 (53): 1227-1236, 2002

13 Fourqurean JW, "Seagrass ecosystems as a globally significant carbon stock" 1 (1): 297-315, 2012

14 Duarte CM, "Seagrass biomass and production:a reassessment" 65 (65): 159-174, 1999

15 Garratt LC, "Salinity tolerance and antioxidant status in cotton cultures" 33 (33): 502-511, 2002

16 Ashraf F, "Roles of glycine betaine and proline in improving plant abiotic stress resistance" 59 (59): 206-216, 2007

17 Doherty CJ, "Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance" 21 (21): 972-984, 2009

18 Wang W, "Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response" 9 (9): 244-252, 2004

19 Tatsumi Y, "Relation between chilling sensitivity of cucurbitaceae fruits and the membrane permeability" 50 (50): 108-113, 2007

20 Apel K, "Reactive oxygen species: metabolism, oxidative stress, and signal transduction" 55 : 373-399, 2004

21 Mittler R, "Reactive oxygen gene network of plants" 9 (9): 490-498, 2004

22 Szabados L, "Proline: a multifunctional amino acid" 15 (15): 89-97, 2010

23 Rajendrakumar CS, "Proline-protein interactions: protection of structural and functional integrity of M4 lactate dehydrogenase" 201 (201): 957-963, 1994

24 Fernández-Bautista N, "Plant tissue trypan blue staining during phytopathogen infection" 2016

25 Thomashow MF, "Plant cold acclimation: freezing tolerance genes and regulatory mechanisms" 50 : 571-599, 1999

26 Scandalios JG, "Oxygen stress and superoxide dismutases" 101 (101): 7-12, 1993

27 Gilmour SJ, "Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation" 124 (124): 1854-1865, 2000

28 Hennessy F, "Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions" 14 (14): 1697-1709, 2005

29 Short FT, "Natural and human-induced disturbance of seagrasses" 23 : 17-27, 1996

30 Zhao C, "Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis" 171 (171): 2744-2759, 2016

31 Trovato M, "Multiple roles of proline in plant stress tolerance and development" 19 (19): 325-346, 2008

32 Sade N, "Measuring Arabidopsis, tomato and barley leaf relative water content (RWC)" 2015

33 Tianzi Chen, "Measurements of Proline and Malondialdehyde Content and Antioxidant Enzyme Activities in Leaves of Drought Stressed Cotton" Bio-Protocol, LLC 6 (6): 2016

34 Oliver ECJ, "Longer and more frequent marine heatwaves over the past century" 9 (9): 1324-, 2018

35 Dutilleul C, "Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation" 15 (15): 1212-1226, 2003

36 Wang D, "Intensification and spatial homogenization of coastal upwelling under climate change" 518 (518): 390-394, 2015

37 Kim M, "Influence of water temperature anomalies on the growth of zostera marina plants held under high and low irradiance levels" 43 (43): 463-476, 2019

38 Georgopoulos CP, "Identification of the E. coli dnaJ gene product" 178 (178): 583-588, 1980

39 Chinnusamy V, "ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis" 17 (17): 1043-1054, 2003

40 Kumar D, "Histochemical detection of superoxide and H2O2 accumulation in Brassica juncea seedlings" 4 (4): 1-, 2014

41 Chen S, "Heat-stress induced expression of stress-inducible nucleotide exchange factor Fes1 in seagrass Zostera japonica" 29 (29): 932-940, 2020

42 Scarpeci TE, "Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes" 66 (66): 361-378, 2008

43 Ito Y, "Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice" 47 (47): 141-153, 2006

44 Ball L, "Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis" 16 (16): 2448-2462, 2004

45 Shi Y, "Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis" 24 (24): 2578-2595, 2012

46 Frölicher TL, "Emerging risks from marine heat waves" 9 (9): 650-, 2018

47 Hiroyuki K, "Effects of aluminum and pH on root growth and cell viability in Arabidopsis thaliana strain landsberg in hydroponic culture" 1 (1): 1-, 1995

48 Shen W, "Effect of Cold Treatment on enzymic and nonenzymic antioxidant activities in leaves of chilling-tolerant and chilling-sensitive cucumber (Cucumis sativus L.)cultivars" 68 (68): 967-973, 1999

49 Anjum F, "Compatibility of osmolytes with Gibbs energy of stabilization of proteins" 1476 (1476): 75-84, 2000

50 Chinnusamy V, "Cold stress regulation of gene expression in plants" 12 (12): 444-451, 2007

51 Thakur P, "Cold stress effects on reproductive development in grain crops: an overview" 67 (67): 429-443, 2010

52 Feng Q, "Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L" 8 : 1042-1052, 2004

53 Kurkela S, "Cloning and characterization of a coldand ABA-inducible Arabidopsis gene" 15 (15): 137-144, 1990

54 Piippo M, "Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress" 25 (25): 142-152, 2006

55 Wilson JM, "Chilling injury in plants" 24 : 445-660, 1987

56 Zhou MQ, "CBF-dependent signaling pathway: a key responder to low temperature stress in plants" 31 (31): 186-192, 2011

57 Fowler S, "Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway" 14 (14): 1675-1690, 2002

58 Rajan VB, "Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors" 9 (9): 433-446, 2009

59 Jaglo-Ottosen KR, "Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance" 280 (280): 104-106, 1998

60 Hodges DM, "Antioxidant enzyme and compound responses to chilling stress and their combining abilities in differentially sensitive maize hybrids" 37 (37): 857-863, 1997

61 Zabta KS, "An ArabidopsisGene family encoding DRE/CRT binding proteins involved in lowtemperature-responsive gene expression" 250 (250): 161-170, 1998

62 Prasad TK, "Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings" 105 (105): 619-627, 1994

63 Waycott M, "Accelerating loss of seagrasses across the globe threatens coastal ecosystems" 106 (106): 12377-12381, 2009

64 Licausi F, "APETALA2/Ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs" 199 (199): 639-649, 2013

65 Junya Mizoi, "AP2/ERF family transcription factors in plant abiotic stress responses" Elsevier BV 1819 (1819): 86-96, 2012

66 Grech A, "A comparison of threats, vulnerabilities and management approaches in global seagrass bioregions" 7 (7): 24006-24013, 2012

67 Agarwal M, "A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance" 281 (281): 37636-37645, 2006