Mitochondria as a target and central hub of energy division during cold stress in insects

Lubawy, Jan; Chowański, Szymon; Adamski, Zbigniew; Słocińska, Małgorzata

doi:10.1186/s12983-021-00448-3

Frontiers in Zoology

Table 1 Changes in genes, energetic parameters of mitochondria and proteins in chill susceptible/chill tolerant or freeze avoiding/tolerant insects after cold/freeze stress

From: Mitochondria as a target and central hub of energy division during cold stress in insects

			Chill susceptible/Chill tolerant		Freeze avoiding/Freeze tolerant
Genes	Acclimated	↑	ATPase (A. colemani) [100]^b	↑↓	COX (E. scudderiana) [35]^c
				↑↓	12S rRNA (E. scudderiana) [35]^c
				↑	HSP60 (D. antiqua) [103]^c
				↓	HSP60 (L. decemlineata) [104]^c
	Non-acclimated	↑	COX (D. simulans) [51]	↑	HSP60 (B. antarctica) [53, 105]
		↑↓	HSP60 (D. melanogaster) [106]	↑	HSP60 (F. occidentalis) [107]
		↑	HSP22 (D. melanogaster) [106]	↑	HSP60 (G. daurica) [108]
		↑	HSP23 (D. melanogaster) [106]	↑	HSP60 (M. alternatus) [109]
		↑	mt:ND4 (D. melanogaster) [52]
		↑	mt:ND5 (D. melanogaster) [52]
		↑↓	mt:COXI (D. melanogaster) [52]
		↑↓	mt:COXII (D. melanogaster) [52]
		↑	UCP4C (D. melanogaster) [54]
		↑↓	HSP23 (D. melanogaster) [110]
		↑	HSP23 (S. crassipalpis) [111]
		↑	AccSCO2 (A. cerana) [112]
		↑	MUP2 (A. melifera) [55]
Energetic parameters	Acclimated	↑	ATP (A. diaperinus) [41]^b	↓	cyt. b (G. groenlandicai) [84]
		↑	TCA (A. colemani) [61]	↓	3-hydroxyacyl-CoA dehydrogenase (E. solidaginis) [79]^c
		↑	citrate (D. melanogaster) [77]	↓	thiolase (E. solidaginis) [79]^c
		↑	aconitate (D. melanogaster) [77]	↓	cyt. c (G. groenlandicai) [44]
		↓	ketoglutarate (D. melanogaster) [77]	↓	CS (C. costata) [76]
		↓	succinate (D. melanogaster) [77]	↓	NAD-IDH (E. solidaginis) [47]^c
		↓	fumarate (D. melanogaster) [77]	↓↑	state 4 (C. costata) [59]^c
		↓	OCR (D. melanogaster) [60]	↑	ATP (C. costata) [59]^c
		↑	ADP/O (D. melanogaster) [60]^a	↑	3-hydroxyacyl-CoA dehydrogenase (E. scudderiana) [79]^c
		↑↓	RCR (D. melanogaster) [60]	↑	thiolase (E. scudderiana) [79]^c
		↓	ATP (D. melanogaster) [60]
		↑	ATP (S. crassipalpis) [44]^b
	Non-acclimated	↓	RCR (G. coquereliana) [89]	↑	NAD-IDH (E. solidaginis) [47]^c
		↓	state 3 (G. coquereliana) [89]	↓	State 4 (C. costata) [59]^c
		↓	OCR (D. melanogaster) [60]	↓	GDH (E. scudderiana) [47]^c
		↑↓	RCR (D. melanogaster) [60]
		↓	ATP (D. melanogaster) [60]
		↓	ATP (S. crassipalpis) [44]
Proteins, enzymes	Acclimated	↑	Aconitase (A. colemani) [61]	↓	COX (E. solidaginis) [47]^c
		↑	Fumarase (A. colemani) [61]	↑	HSP70 (E. solidaginis) [113]^b,^c
		↑	Malate dehydrogenase (A. colemani) [61]	↑↓	HSP70 (E. solidaginis) [113]^c
				↓	COX (E. scudderiana) [35, 47]^c
				↑↓	SOD (E. solidaginis) [114]^c
				↑	SOD (E. scudderiana) [114]^c
	Non-acclimated	↓	GSHt (A. diaperinus) [115]
		↑	UCP (G. coquereliana) [89]
		↑	HSP70 (G. coquereliana) [89, 116]
		↑	HSP70 (S. exigua) [117]
		↓	HSP60 (S. exigua) [117]
		↓↑	procaspase-9-like (D. melanogaster) [58]
		↓↑	caspase-3-like (D. melanogaster) [58]
		↓	Bcl-2 (D. melanogaster) [58]

The table is divided also into research on insects acclimated to low temperatures (acclimated) and insects not acclimated to low temperatures (non-acclimated). Empty cells in the table indicate that research in this direction has not been conducted and much is still to unravel. As each division would be artificial, we decided to rank insects into species in which cold-induced injury, and death occurs at temperatures above temperature causing extracellular freezing (Chill susceptible/Chill tolerant) and species in which injury is related to ice formation (Freeze avoiding/Freeze tolerant) (for review see Overgaard and MacMillan [27]). Arrows indicate: ↑ increase/up-regulation, ↓ decrease/down-regulation, ↑↓ no change
^aCompared to non-acclimated counter partners
^bFTR or freeze–thaw cycles were used in the studies and not cold-acclimation per se
^cDiapausing insects

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