Symbiosis with Dinoflagellates Alters Cnidarian Cell-Cycle Gene Expression

Table 1

Differentially expressed host cell-cycle genes between symbiotic states and host tissues in Aiptasia. Numbers represent log-fold change in expression between samples.

Gene	Cell-cycle stage	Role	References	Aiptasia transcript ID	Symbiotic gastrodermis vs aposymbiotic gastrodermis	Symbiotic gastrodermis vs epidermis of symbiotic hosts	Epidermis of symbiotic vs aposymbiotic hosts	Aposymbiotic gastrodermis vs epidermis of aposymbiotic hosts
ATM/ATR	S	DNA damage response proteins that check for DNA damage during DNA replication; activation leads to apoptosis and cell-cycle arrest at the S and G2/M checkpoints and DNA repair	[41]; [66]	AIPGENE9815		−0.821
Bub1	G2	Forms the mitotic checkpoint complex (MCC); MCC produces the “wait anaphase” signal and inhibits the anaphase promoting complex APC/C by directly phosphorylating its activator (Cdc20) in the interphase, allowing the accumulation of cyclin B in the G2 phase and inhibiting mitotic exit	[67]; [68]; [69]; [70]; [71]; [72]; [73]	AIPGENE2130	−0.833
Cdc14A phosphatase	M	Regulation of the G2/damage checkpoint and essential for the exit from mitosis by dephosphorylation of CDK1 substrates—mitotic cyclins; indirect role during DNA replication by suppressing CDKs upon mitotic exit, allowing the effective formation of pre-RC complexes during the S phase	[74]; [75]; [76]; [77]; [78]	AIPGENE20570	1.492			−0.584
Cdc20	M	Activator of anaphase-promoting complex (APC/C) which initiates chromosome separation and subsequently destroys cyclin B and deactivates CDK1, allowing the exit from mitosis and the completion of the cell cycle	[79]; [70]	AIPGENE561	−1.489
Cdc25B,C	G2/M	Phosphorylation of Cdc25B activates the cyclin B-CDK1 complexes whose activity remains high until anaphase	[80]; [81]; [82]	AIPGENE19331	−1.022
Cyclin B	M	Forms complex with CDK1 in mitosis and required for mitotic progression	[83]	AIPGENE10534	−1.255
CDK1	G2/M	Forms complex with cyclin A in the G2 phase to fortify cells for commitment to mitosis as it is an upstream regulator of Plk1; forms complex with cyclin B in the M phase for mitotic progression	[84]	AIPGENE3823	−1.644
CDK4,6	G1	Regulator of the restriction point in G1 through phosphorylation of the Rb-E2F complex	[85]	AIPGENE14397	−0.782
c-Myc	G0	Cell-cycle entry of quiescent (G0) cells and increasing apoptotic sensitivity by amplifying death receptor pathways	[86]; [87]; [88]; [89]; [90]	AIPGENE2563		−3.550
				AIPGENE2519		−1.052
Dp-1,2	G1/S	Makes complexes with E2F transcription factors that then bind to different proteins and changes their function for cell-cycle progression	[91]	AIPGENE10647	1.356
				AIPGENE22485	1.439	1.881
				AIPGENE22512	−0.596
E2F1,2,3	G0 to S	G0 to S phase progression; DNA stability; transcriptional activators of essential cell-cycle genes	[91]	AIPGENE28094		1.287
GADD45	G2/M	Inhibitor of cyclin B/CDK1; apoptosis; cell-cycle arrest	[92]; [93]	AIPGENE19027	0.914
HDAC1	G1/S	Repress transcription through the deacetylation of lysine residues on histones, changing chromatin conformation and actively stopping protein function	[94]	AIPGENE13245	0.713
Mcm3	S	Forms MCM helicase complex that is required during DNA replication; loaded onto chromatin by the origin recognition complex (ORC) at the sites of replication during the G1 phase; unwinds DNA; elicits replication and elongation; strict localization and timings to ensure that DNA replication only occurs once per cell cycle	[95]; [96]; [97]; [98]	AIPGENE29020	−0.675	−0.799
Mcm6				AIPGENE8456	−0.859
Mdm2	G2/M	Antagonistic controller of p53 and inhibits its role in apoptotic initiation and the G1 arrest; delays cell-cycle progression in the G2/M phase	[99]; [100]; [101]; [102]	AIPGENE26697	1.111	0.889
Mob1	M	Cell polarity marker involved in the mitotic exit network (MEN) signalling cascade and associates with spindle pole bodies throughout the cell cycle	[103]	AIPGENE20640			0.979
Mps1	M	Forms the mitotic checkpoint complex (MCC); MCC produces the “wait anaphase” signal and inhibits the anaphase promoting complex APC/C by directly phosphorylating its activator (Cdc20) in the interphase, allowing the accumulation of cyclin B in the G2 phase and inhibiting mitotic exit	[67]; [68]; [69]; [70]; [71]; [72]; [73]	AIPGENE12491	−0.920
ORC3	S	Forms the ORC (origin recognition complex) and binds to replicating sequences in the chromatin, allowing the attachment of other replication proteins, e.g., MCM-helicase	[104]; [96]; [105]	AIPGENE5780				−0.675
Plk1	M	Promotes mitotic entry by inducing the phosphorylation of Cdc25B/C and is the kinase required for mitotic spindle function in chromosome separation	[106]; [84]	AIPGENE7783	−0.583
				AIPGENE16487		−2.327
p27 kip1	G1/S	CDK inhibitor that binds to CDK 2-cyclin E complexes at the G1/S phase to inhibit cell-cycle progression	[107]; [108]	AIPGENE22427				−0.770
SCF (Skp1/Cullin/F-; Box protein)	G1/S	E3 ubiquitin ligase involved in controlling the progression of the cell cycle by degrading cell-cycle antagonists, e.g., p57, p27, p21, Wee1, and Emi1; regulates entry into the S phase with increasing levels destroying S-phase antagonists p21and p27, allowing the cells to enter the S phase	[109]; [110]; [111]; [112]	AIPGENE5823 (Cullin-1)	0.504
				AIPGENE15738 (S-phase associated kinase)	1.180
				AIPGENE15719 (S-phase associated kinase)	−0.902
14-3-3 protein	G2/M	Regulates Cdc25B/C	[80]	AIPGENE804	−0.479