Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model

被引:106
作者
Norouzitallab, Parisa [1 ,2 ]
Baruah, Kartik [1 ,2 ]
Vandegehuchte, Michiel [3 ]
Van Stappen, Gilbert [1 ,2 ]
Catania, Francesco [4 ]
Vanden Bussche, Julie [5 ]
Vanhaecke, Lynn [5 ]
Sorgeloos, Patrick [1 ,2 ]
Bossier, Peter [1 ,2 ]
机构
[1] Univ Ghent, Lab Aquaculture, B-9000 Ghent, Belgium
[2] Univ Ghent, Artemia Reference Ctr, B-9000 Ghent, Belgium
[3] Univ Ghent, Lab Environm Toxicol & Aquat Ecol, B-9000 Ghent, Belgium
[4] Univ Munster, Inst Evolut & Biodivers, D-48149 Munster, Germany
[5] Univ Ghent, Chem Anal Lab, Merelbeke, Belgium
关键词
heat shock protein 70; DNA methylation; histone modification; stress resistance; heritability; SHOCK-PROTEIN; 70S; HISTONE MODIFICATIONS; GENOME INSTABILITY; DNA METHYLATION; HSP70; GENE; FRANCISCANA; TEMPERATURE; ACETYLATION; ARABIDOPSIS; RESISTANCE;
D O I
10.1096/fj.14-252049
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The notion that phenotypic traits emerging from environmental experiences are heritable remains under debate. However, the recent report of nonmendelian transgenerational epigenetic inheritance, i.e., the inheritance of traits not determined by the DNA sequence, might make such a phenomenon plausible. In our study, by carrying out common garden experiments, we could provide clear evidences that, on exposure to nonlethal heat shocks, a parental population of parthenogenetic (all female) Artemia (originating from one single female) experiences an increase in levels of Hsp70 production, tolerance toward lethal heat stress, and resistance against pathogenic Vibrio campbellii. Interestingly, these acquired phenotypic traits were transmitted to three successive generations, none of which were exposed to the parental stressor. This transgenerational inheritance of the acquired traits was associated with altered levels of global DNA methylation and acetylated histones H3 and H4 in the heat-shocked group compared to the control group, where both the parental and successive generations were reared at standard temperature. These results indicated that epigenetic mechanisms, such as global DNA methylation and histones H3 and H4 acetylation, have particular dynamics that are crucial in the heritability of the acquired adaptive phenotypic traits across generations.
引用
收藏
页码:3552 / 3563
页数:12
相关论文
共 71 条
[1]   Effects of salinity and temperature on reproductive and life span characteristics of clonal Artemia.: (International Study on Artemia.: LXVI) [J].
Abatzopoulos, TJ ;
El-Bermawi, N ;
Vasdekis, C ;
Baxevanis, AD ;
Sorgeloos, P .
HYDROBIOLOGIA, 2003, 492 (1-3) :191-199
[2]   Epigenetics and environment: a complex relationship [J].
Aguilera, Oscar ;
Fernandez, Agustin F. ;
Munoz, Alberto ;
Fraga, Mario F. .
JOURNAL OF APPLIED PHYSIOLOGY, 2010, 109 (01) :243-251
[3]   Plant molecular stress responses face climate change [J].
Ahuja, Ishita ;
de Vos, Ric C. H. ;
Bones, Atle M. ;
Hall, Robert D. .
TRENDS IN PLANT SCIENCE, 2010, 15 (12) :664-674
[4]   Epigenetic transgenerational actions of endocrine disruptors and mate fertility [J].
Anway, MD ;
Cupp, AS ;
Uzumcu, M ;
Skinner, MK .
SCIENCE, 2005, 308 (5727) :1466-1469
[5]   Feeding truncated heat shock protein 70s protect Artemia franciscana against virulent Vibrio campbellii challenge [J].
Baruah, Kartik ;
Norouzitallab, Parisa ;
Li Shihao ;
Sorgeloos, Patrick ;
Bossier, Peter .
FISH & SHELLFISH IMMUNOLOGY, 2013, 34 (01) :183-191
[6]   A novel heat-shock protein inducer triggers heat shock protein 70 production and protects Artemia franciscana nauplii against abiotic stressors [J].
Baruah, Kartik ;
Norouzitallab, Parisa ;
Roberts, Ronald J. ;
Sorgeloos, Patrick ;
Bossier, Peter .
AQUACULTURE, 2012, 334 :152-158
[7]   Priming the prophenoloxidase system of Artemia franciscana by heat shock proteins protects against Vibrio campbellii challenge [J].
Baruah, Kartik ;
Ranjan, Jayant ;
Sorgeloos, Patrick ;
MacRae, Thomas H. ;
Bossier, Peter .
FISH & SHELLFISH IMMUNOLOGY, 2011, 31 (01) :134-141
[8]   Efficacy of heterologous and homologous heat shock protein 70s as protective agents to Artemia franciscana challenged with Vibrio campbellii [J].
Baruah, Kartik ;
Ranjan, Jayant ;
Sorgeloos, Patrick ;
Bossier, Peter .
FISH & SHELLFISH IMMUNOLOGY, 2010, 29 (05) :733-739
[9]  
Baxevanis Athanasios D., 2004, Journal of Biological Research (Thessaloniki), V1, P107
[10]   Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life [J].
Benyshek, DC ;
Johnston, CS ;
Martin, JF .
DIABETOLOGIA, 2006, 49 (05) :1117-1119