

FOLLOWUS
1. School of Biology & Basic Medical Sciences, Soochow University, Suzhou 215101, China
2. Department of Pathology, Affiliated Hospital and Medical School of Nantong University, Nantong 226001, China
shensongdong@suda.edu.cn
Received:24 August 2023,
Online First:04 November 2023,
Published:01 July 2024
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HE Hongyan,YANG Juanjuan,HE Yuan,et al.Proliferating cell nuclear antigen of Ulva, prolifera is involved in the response to temperature stress[J].Journal of Oceanology and Limnology,2024,42(04):1227-1241.
Ulva
prolifera
is the most common specie causative to green tide
and its growth is sensitive to temperature stress. However
the mechanisms of
U
.
prolifera
response to temperature stress remain elusive. In this study
high temperature (36 °C) stimulus promoted the death of unformed cell wall protoplasts and delayed the division of formed cell wall protoplasts
while low-temperature (4 °C) stimulus did not
suggesting that the mechanisms of the response of
U
.
prolifera
to high and low-temperature stresses are different. Transcriptome results show that proliferation-related genes were differentially expressed under high and low-temperature stresses
especially the proliferating cell nuclear antigen (PCNA) and cyclins (CYCs). Subsequently
the interaction between PCNA and Cyclin A was confirmed by Co-immunoprecipitation
yeast two-hybrid
and so on. Furthermore
high- and low-temperature stresses induced the expression of
PCNA
and
Cyclin
A
in varying of degrees
and activated extracellular signal-regulated kinase (ERK) signal pathway. These results suggest
PCNA
Cyclin
A
and ERK signal pathway played important roles in the resistance of
U
.
prolifera
to temperature stress. Interestingly
high-temperature stress induced an increase of miR-2916 in abundance
and exhibiting reverse expression of
PCNA
; and PCNA was target gene of miR-2916
suggesting that miR-2916 protected
U
.
prolifera
from high-temperature stress via post-transcriptionally regulation of PCNA. This study laid a foundation for understanding the function of
PCNA
and
Cyclin
A
moreover
it has a guiding significance to explore the mechanisms of the response to temperature stress from proliferation-related genes regulatory networks in
U
.
prolifera
.
Atkins K C , Cross F R . 2018 . Interregulation of CDKA/CDK1 and the plant-specific cyclin-dependent kinase CDKB in control of the Chlamydomonas cell cycle . The Plant Cell , 30 ( 2 ): 429 - 446 , https://doi.org/10.1105/tpc.17.00759 https://doi.org/10.1105/tpc.17.00759 .
Banerjee G , Singh D , Sinha A K . 2020 . Plant cell cycle regulators: mitogen-activated protein kinase, a new regulating switch? Plant Science , 301 : 110660 , https://doi.org/10.1016/j.plantsci.2020.110660 https://doi.org/10.1016/j.plantsci.2020.110660 .
Bergink S , Jentsch S . 2009 . Principles of ubiquitin and SUMO modifications in DNA repair . Nature , 458 ( 7237 ): 461 - 467 , https://doi.org/10.1038/nature07963 https://doi.org/10.1038/nature07963 .
Billoud B , Nehr Z , Le Bail A et al . 2014 . Co mputational prediction and experimental validation of microRNAs in the brown alga Ectocarpus siliculosus . Nucleic Acids Research , 42 ( 1 ): 417 - 429 , https://doi.org/10.1093/nar/gkt856 https://doi.org/10.1093/nar/gkt856 .
Čížková M , Pichová A , Vítová M et al . 2008 . CDKA and CDKB kinases from Chlamydomonas reinhardtii are able to complement cdc 28 temperature-sensitive mutants of Saccharomyces cerevisiae . Protoplasma , 232 ( 3 ): 183 - 191 , https://doi.org/10.1007/s00709-008-0285-z https://doi.org/10.1007/s00709-008-0285-z .
De Biasio A , Blanco F J . 2013b . Proliferating cell nuclear antigen structure and interactions: too many partners for one dancer? Advances in Protein Chemistry and Structural Biology , 91 : 1 - 36 , https://doi.org/10.1016/B978-0-12-411637-5.00001-9 https://doi.org/10.1016/B978-0-12-411637-5.00001-9 .
Dewitte W , Murray J A H . 2003 . The plant cell cycle . Annual Review of Plant Biology , 54 : 235 - 264 , https://doi.org/10.1146/annurev.arplant.54.031902.134836 https://doi.org/10.1146/annurev.arplant.54.031902.134836 .
Dittami S M , Duboscq-Bidot L , Perennou M et al . 2016 . Host-microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures . Isme Journal , 10 ( 1 ): 51 - 63 , https://doi.org/10.1038/ismej.2015.104 https://doi.org/10.1038/ismej.2015.104 .
Fan M H , Sun X , Liao Z et al . 2018 . Comparative proteomic analysis of Ulva prolifera response to high temperature stress . Proteome Science , 16 ( 1 ): 17 , https://doi.org/10.1186/s12953-018-0145-5 https://doi.org/10.1186/s12953-018-0145-5 .
Fletcher R L , Callow M E . 1992 . The settlement, attachment and establishment of marine algal spores . British Phycological Journal , 27 ( 3 ): 303 - 329 , https://doi.org/10.1080/00071619200650281 https://doi.org/10.1080/00071619200650281 .
Fu G , Yao J T , Liu F L et al . 2008 . Effect of temperature and irradiance on the growth and reproduction of Enteromorpha prolifera J. Ag. (Chlorophycophyta, Chlorophyceae) . Chinese Journal of Oceanology and Limnology , 26 ( 4 ): 357 - 362 , https://doi.org/10.1007/s00343-008-0357-0 https://doi.org/10.1007/s00343-008-0357-0 .
Ghaderiardakani F , Langhans L , Kurbel V B et al . 2022 . Metabolite profiling reveals insights into the species-dependent cold stress response of the green seaweed holobiont Ulva (Chlorophyta) . Environmental and Experimental Botany , 200 : 104913 , https://doi.org/10.1016/j.envexpbot.2022.104913 https://doi.org/10.1016/j.envexpbot.2022.104913 .
Ghaderiardakani F , Quartino M L , Wichard T . 2020 . Microbiome-dependent adaptation of seaweeds under environmental stresses: a perspective . Frontiers in Marine Science , 7 : 575228 , https://doi.org/10.3389/fmars.2020.575228 https://doi.org/10.3389/fmars.2020.575228 .
Giacomelli J I , Weigel D , Chan R L et al . 2012 . Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage . New Phytologist , 195 ( 4 ): 766 - 773 , https://doi.org/10.1111/j.1469-8137.2012.04259.x https://doi.org/10.1111/j.1469-8137.2012.04259.x .
Hackenberg M , Gustafson P , Langridge P et al . 2015 . Differential expression of microRNAs and other small RNAs in barley between water and drought conditions . Plant Biotechnology Journal , 13 ( 1 ): 2 - 13 , https://doi.org/10.1111/pbi.12220 https://doi.org/10.1111/pbi.12220 .
He Y , Yan Z H , Du Y et al . 2017 . Molecular cloning and expression analysis of two key genes, HDS and HDR, in the MEP pathway in Pyropia haitanensis . Scientific Reports , 7 ( 1 ): 17499 , https://doi.org/10.1038/s41598-017-17521-9 https://doi.org/10.1038/s41598-017-17521-9 .
He Y L , Hu C Y , Wang Y H et al . 2018 . The metabolic survival strategy of marine macroalga Ulva prolifera under temperature stress . Journal of Applied Phycology , 30 ( 6 ): 3611 - 3621 , https://doi.org/10.1007/s10811-018-1493-3 https://doi.org/10.1007/s10811-018-1493-3 .
Hmani I , Ghaderiardakani F , Ktari L et al . 2023 . High-temperature stress induces bacteria-specific adverse and reversible effects on Ulva (Chlorophyta) growth and its chemosphere in a reductionist model system . Botanica Marina , https://doi.org/10.1515/bot-2023-0053 https://doi.org/10.1515/bot-2023-0053 .
Huang A Y , Wang G C , He L W et al . 2011 . Characterization of small RNAs from Ulva prolifera by high-throughput sequencing and bioinformatics analysis . Chinese Science Bulletin , 56 ( 27 ): 2916 - 2921 , https://doi.org/10.1007/s11434-011-4678-6 https://doi.org/10.1007/s11434-011-4678-6 .
Jiménez C , Cossío B R , Rivard C J et al . 2007 . Cell division in the unicellular microalga Dunaliella viridis depends on phospho rylation of extracellular signal-regulated kinases (ERKs) . Journal of Experimental Botany , 58 ( 5 ): 1001 - 1011 , https://doi.org/10.1093/jxb/erl260 https://doi.org/10.1093/jxb/erl260 .
Ju Z , Cao D Y , Gao C et al . 2017 . A viral satellite DNA vector (TYLCCNV) for functional analysis of miRNAs and siRNAs in plants . Plant Physiology , 173 ( 4 ): 1940 - 1952 , https://doi.org/10.1104/pp.16.01489 https://doi.org/10.1104/pp.16.01489 .
Kalapos B , Hlavová M , Nádai T V et al . 2019 . Early evolution of the mitogen-activated protein kinase family in the plant kingdom . Scientific Reports , 9 ( 1 ): 4094 , https://doi.org/10.1038/s41598-019-40751-y https://doi.org/10.1038/s41598-019-40751-y .
Kirkendale L , Saunders G W , Winberg P . 2013 . A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism . Journal of Phycology , 49 ( 1 ): 69 - 81 , https://doi.org/10.1111/jpy.12016 https://doi.org/10.1111/jpy.12016 .
Koundrioukoff S , Jónsson Z A O , Hasan S et al . 2000 . A direct interaction between proliferating cell nuclear antigen (PCNA) and cdk2 targets PCNA-interacting proteins for phosphorylation . Journal of Biological Chemistry , 275 ( 30 ): 22882 - 22887 , https://doi.org/10.1074/jbc.M001850200 https://doi.org/10.1074/jbc.M001850200 .
Kruszka K , Pacak A , Swida-Barteczka A et al . 2014 . Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley . Journal of Experimental Botany , 65 ( 20 ): 6123 - 6135 , https://doi.org/10.1093/jxb/eru353 https://doi.org/10.1093/jxb/eru353 .
Li J , Wu L Q , Zheng W Y et al . 2015 . Genome-wide identification of microRNAs responsive to high temperature in Rice ( Oryza sativa ) by high-throughput deep sequencing . Journal of Agronomy and Crop Science , 201 ( 5 ): 379 - 388 , https://doi.org/10.1111/jac.12114 https://doi.org/10.1111/jac.12114 .
Li Y X , Zhang X W , Xu D et al . 2012 . Differential gene expression in Ulva prolifera under low light and low temperature conditions . Current Genetics , 58 ( 4 ): 235 - 244 , https://doi.org/10.1007/s00294-012-0380-8 https://doi.org/10.1007/s00294-012-0380-8 .
Liu F , Pang S J , Zhao X B et al . 2012 . Quantitative, molecular and growth analyses of Ulva microscopic propagules in the coastal sediment of Jiangsu province where green tides initially occurred . Marine Environmental Research , 74 : 56 - 63 , https://doi.org/10.1016/j.marenvres.2011.12.004 https://doi.org/10.1016/j.marenvres.2011.12.004 .
Liu X J , Blomme J , Bogaert K A et al . 2022 . Transcriptional dynamics of gametogenesis in the green seaweed Ulva mutabilis identifies an RWP-RK transcription factor linked to reproduction . BMC Plant Biology , 22 ( 1 ): 19 , https://doi.org/10.1186/s12870-021-03361-3 https://doi.org/10.1186/s12870-021-03361-3 .
May P , Liao W , Wu Y J et al . 2013 . The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development . Nature Communications , 4 ( 1 ): 2145 , https://doi.org/10.1038/ncomms3145 https://doi.org/10.1038/ncomms3145 .
Metaxa E , Deviller G , Pagand P et al . 2006 . High rate algal pond treatment for water reuse in a marine fish recirculation system: water purification and fish health . Aquaculture , 252 ( 1 ): 92 - 101 , https://doi.org/10.1016/j.aquaculture.2005.11.053 https://doi.org/10.1016/j.aquaculture.2005.11.053 .
Niu J , Wang J , An J Y et al . 2016 . Integrated mRNA and miRNA transcriptome reveal a cross-talk between developing response and hormone signaling for the seed kernels of Siberian apricot . Scientific Reports , 6 ( 1 ): 35675 , https://doi.org/10.1038/srep35675 https://doi.org/10.1038/srep35675 .
Parages M L , Figueroa F L , Conde-Álvarez R M et al . 2014 . Phosphorylation of MAPK-like proteins in three intertidal macroalgae under stress conditions . Aquatic Biology , 22 : 213 - 226 , https://doi.org/10.3354/ab00592 https://doi.org/10.3354/ab00592 .
Park S Y , Fung P , Nishimura N et al . 2009 . Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins . Science , 324 ( 5930 ): 1068 - 1071 , https://doi.org/10.1126/science.1173041 https://doi.org/10.1126/science.1173041 .
Qian J , Chen Y Y , Xu Y X et al . 2019 . Interactional similarities and differences in the protein complex of PCNA and DNA replication factor C between rice and Arabidopsis . BMC Plant Biology , 19 ( 1 ): 257 , https://doi.org/10.1186/s12870-019-1874-z https://doi.org/10.1186/s12870-019-1874-z .
Raynaud C , Sozzani R , Glab N et al . 2006 . Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis . Plant Journal , 47 ( 3 ): 395 - 407 , https://doi.org/10.1111/j.1365-313X.2006.02799.x https://doi.org/10.1111/j.1365-313X.2006.02799.x .
Roig E G , Vázquez-Ramos J M . 2003 . Maize DNA polymerase alpha is phosphorylated by a PCNA-associated cyclin/Cdk complex: effect of benzyladenine . Journal of Plant Physiology , 160 ( 9 ): 983 - 990 , https://doi.org/10.1078/0176-1617-01088 https://doi.org/10.1078/0176-1617-01088 .
Provasoli L . Media and prospects for the cultivation of marine algae [J ] . Cultures and Collections of Algae , 1968 : 63 - 75 .
Sánchez M D L , Gurusinghe S H , Bradford K J et al . 2005 . Differential response of PCNA and Cdk-A proteins and associated kinase activities to benzyladenine and abscisic acid during maize seed germination . Journal of Experimental Botany , 56 ( 412 ): 515 - 523 , https://doi.org/10.1093/jxb/eri029 https://doi.org/10.1093/jxb/eri029 .
Sasabe M , Machida Y . 2012 . Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis . Cytoskeleton , 69 ( 11 ): 913 - 918 , https://doi.org/10.1002/cm.21072 https://doi.org/10.1002/cm.21072 . https://do 10.1002/cm.21072 http://dx.doi.org/10.1002/cm.21072
Schories D . 1995 . Sporulation of Enteromorpha spp. (Chlorophyta) and overwintering of spores in sediments of the Wadden Sea, Island Sylt, North Sea . Netherland Journal of Aquatic Ecology , 29 ( 3-4 ): 341 - 347 , https://doi.org/10.1007/bf02084233 https://doi.org/10.1007/bf02084233 .
Strzalka W , Ziemienowicz A . 2011 . Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation . Annals of Botany , 107 ( 7 ): 1127 - 1140 , https://doi.org/10.1093/aob/mcq243 https://doi.org/10.1093/aob/mcq243 .
Tarver J E , Cormier A , Pinzón N et al . 2015 . microRNAs and the evolution of complex multicellularity: identification of a large, diverse complement of microRNAs in the brown alga Ectocarpus . Nucleic Acids Research , 43 ( 13 ): 6384 - 6398 , https://doi.org/10.1093/nar/gkv578 https://doi.org/10.1093/nar/gkv578 .
Wang Y , Wang Y , Zhu L et al . 2012 . Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions . PLoS One , 7 ( 8 ): e38245 , https://doi.org/10.1371/journal.pone.0038245 https://doi.org/10.1371/journal.pone.0038245 .
Wichard T . 2023 . From model organism to application: bacteria-induced growth and development of the green seaweed Ulva and the potential of microbe leveraging in algal aquaculture . Seminars in Cell & Developmental Biology , 134 : 69 - 78 , https://doi.org/10.1016/j.semcdb.2022.04.007 https://doi.org/10.1016/j.semcdb.2022.04.007 .
Worm B , Lotze H K . 2006 . Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnology and Oceanography , 51 (1part 2 ): 569 - 579 , https://doi.org/10.4319/lo.2006.51.1_part_2.0569 https://doi.org/10.4319/lo.2006.51.1_part_2.0569 . https://do 10.4319/lo.2006.51.1_part_2.0569 http://dx.doi.org/10.4319/lo.2006.51.1_part_2.0569
Xin M M , Wang Y , Yao Y Y et al . 2010 . Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat ( Triticum aestivum L.) . BMC Plant Biology , 10 ( 1 ): 123 , https://doi.org/10.1186/1471-2229-10-123 https://doi.org/10.1186/1471-2229-10-123 . https://do 10.1186/1471-2229-10-123 http://dx.doi.org/10.1186/1471-2229-10-123
Yang C H , Li D Y , Mao D H et al . 2013 . Overexpression of microRNA319 impacts lea f morphogenesis and leads to enhanced cold tolerance in rice ( Oryza sativa L.) . Plant, Cell & Environment , 36 ( 12 ): 2207 - 2218 , https://doi.org/10.1111/pce.12130 https://doi.org/10.1111/pce.12130 . https://do 10.1111/pce.12130 http://dx.doi.org/10.1111/pce.12130
Yang J J , Yin Y , Yu D C et al . 2021 . Activation of MAPK signaling in response to nitrogen deficiency in Ulva prolifera ( Chlorophyta ) . Algal Research , 53 : 102153 , https://doi.org/10.1016/j.algal.2020.102153 https://doi.org/10.1016/j.algal.2020.102153 .
Yang J J , Yu D C , Ma Y F et al . 2019 . Antioxidative defense response of Ulva prolifera under high or low-temperature stimulus . Algal Research , 44 : 101703 , https://doi.org/10.1016/j.algal.2019.101703 https://doi.org/10.1016/j.algal.2019.101703 .
Zachleder V , Ivanov I , Vítová M et al . 2019 . Cell cycle arrest by supraoptimal temperature in the alga Chlamydomonas reinhardtii . Cells , 8 ( 10 ): 1237 , https://doi.org/10.3390/cells8101237 https://doi.org/10.3390/cells8101237 .
Zhao C , Sun Y , Yi Z C et al . 2010 . Simulated microgravity inhibits cell wall regeneration of Penicillium decumbens protoplasts . Advances in Space Research , 46 ( 6 ): 701 - 706 , https://doi.org/10.1016/j.asr.2010.04.026 https://doi.org/10.1016/j.asr.2010.04.026 .
Zhou Y , Fowke L , Wang H . 2002 . Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants . Plant Cell Reports , 20 ( 10 ): 967 - 975 , https://doi.org/10.1007/s00299-001-0434-8 https://doi.org/10.1007/s00299-001-0434-8 .
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