Cryopreserved-pollen viability is regulated by NO-induced programmed cell death
Key message After cryopreservation, the NO content in pollen increased, inducing programmed cell death as a key reason for reduced viability. Low recovery of biomaterials after cryopreservation is a bottleneck that limits the application of this technology. At present, the mechanism of viability dec...
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| Veröffentlicht in: | Plant cell reports 2021-12, Vol.40 (12), p.2383-2395 |
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| creator | Ren, Ruifen Zhou, Hao Zhang, Lingling Jiang, Xueru Liu, Yan |
| description | Key message
After cryopreservation, the NO content in pollen increased, inducing programmed cell death as a key reason for reduced viability.
Low recovery of biomaterials after cryopreservation is a bottleneck that limits the application of this technology. At present, the mechanism of viability decline after cryopreservation is not fully understood. In this study, the effects of nitric oxide (NO) on programmed cell death (PCD) and its relationship with viability were investigated, using
Paeonia lactiflora
'Fen Yu Nu' pollen with significantly decreased viability after cryopreservation. The results showed that: the activity of caspase-3-like and caspase-9-like protease and the apoptosis rate of pollen cells were significantly increased, the expression level of the promoting PCD (pro-PCD) genes was up-regulated, while the expression level of the inhibiting PCD (anti-PCD) genes was down-regulated after preservation in liquid nitrogen (LN); the NO content in pollen cells increased significantly after LN exposure. The correlation analysis showed that NO was significantly correlated with pollen viability and all indicators of PCD. The addition of a NO carrier SNP after LN storage reduced pollen viability, increased endogenous NO content, decreased mitochondrial membrane potential level, activated caspase-3-like and caspase-9-like protease in pollen cells, and increased cell apoptosis rate. The expression levels of pro-PCD genes
PDCD2
and
ATG8CL
were significantly up-regulated, while the expression levels of anti-PCD genes
DAD1
,
BI-1
and
LSD1
were significantly down-regulated. The addition of NO scavenger c-PTIO improved pollen viability, and produced the opposite effect of sodium nitroferricyanide (III) dihydrate (SNP), but did not change the mitochondrial membrane potential. These results suggest that NO induced PCD during the cryopreservation of pollen, which was one of the reasons for the significant decrease of pollen viability after cryopreservation. |
| doi_str_mv | 10.1007/s00299-021-02779-1 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2566261513</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2566261513</sourcerecordid><originalsourceid>FETCH-LOGICAL-c375t-87c43769cee216af5e21a300e2938b9ac978cf9dacff8d41897af7fe5b345d6c3</originalsourceid><addsrcrecordid>eNp9kEtLxDAUhYMozjj6B1xIwY2bah5tHksZfMHgbBTchTS9HTv0MSbtQP-9GTsquHARbsL57snhIHRO8DXBWNx4jKlSMaYkHCFUTA7QlCSMxhSzt0M0xSJIQpBkgk68X2McRMGP0YQlSaoUJ1O0nLuh3Tjw4LaQx5u2qqCJtqXJyqrshqj0kYNVX5kO8igboudlXDZ5b8Nr49qVM3UdrhaqKsrBdO-n6KgwlYez_Zyh1_u7l_ljvFg-PM1vF7FlIu1iKewuirIAlHBTpGEYhjFQxWSmjFVC2kLlxhaFzBMilTCFKCDNWJLm3LIZuhp9Q4qPHnyn69LvYpgG2t5rmnJOOUkJC-jlH3Td9q4J6QKluCRMSBkoOlLWtd47KPTGlbVxgyZY7-rWY9061K2_6tYkLF3srfss9PCz8t1vANgI-CA1K3C_f_9j-wm4bYr9</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2596813788</pqid></control><display><type>article</type><title>Cryopreserved-pollen viability is regulated by NO-induced programmed cell death</title><source>MEDLINE</source><source>Springer Nature - Complete Springer Journals</source><creator>Ren, Ruifen ; Zhou, Hao ; Zhang, Lingling ; Jiang, Xueru ; Liu, Yan</creator><creatorcontrib>Ren, Ruifen ; Zhou, Hao ; Zhang, Lingling ; Jiang, Xueru ; Liu, Yan</creatorcontrib><description>Key message
After cryopreservation, the NO content in pollen increased, inducing programmed cell death as a key reason for reduced viability.
Low recovery of biomaterials after cryopreservation is a bottleneck that limits the application of this technology. At present, the mechanism of viability decline after cryopreservation is not fully understood. In this study, the effects of nitric oxide (NO) on programmed cell death (PCD) and its relationship with viability were investigated, using
Paeonia lactiflora
'Fen Yu Nu' pollen with significantly decreased viability after cryopreservation. The results showed that: the activity of caspase-3-like and caspase-9-like protease and the apoptosis rate of pollen cells were significantly increased, the expression level of the promoting PCD (pro-PCD) genes was up-regulated, while the expression level of the inhibiting PCD (anti-PCD) genes was down-regulated after preservation in liquid nitrogen (LN); the NO content in pollen cells increased significantly after LN exposure. The correlation analysis showed that NO was significantly correlated with pollen viability and all indicators of PCD. The addition of a NO carrier SNP after LN storage reduced pollen viability, increased endogenous NO content, decreased mitochondrial membrane potential level, activated caspase-3-like and caspase-9-like protease in pollen cells, and increased cell apoptosis rate. The expression levels of pro-PCD genes
PDCD2
and
ATG8CL
were significantly up-regulated, while the expression levels of anti-PCD genes
DAD1
,
BI-1
and
LSD1
were significantly down-regulated. The addition of NO scavenger c-PTIO improved pollen viability, and produced the opposite effect of sodium nitroferricyanide (III) dihydrate (SNP), but did not change the mitochondrial membrane potential. These results suggest that NO induced PCD during the cryopreservation of pollen, which was one of the reasons for the significant decrease of pollen viability after cryopreservation.</description><identifier>ISSN: 0721-7714</identifier><identifier>EISSN: 1432-203X</identifier><identifier>DOI: 10.1007/s00299-021-02779-1</identifier><identifier>PMID: 34459961</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Apoptosis ; Apoptosis - genetics ; Biomaterials ; Biomedical and Life Sciences ; Biomedical materials ; Biotechnology ; Caspase-3 ; Caspase-9 ; Caspases - metabolism ; Cell Biology ; Cell death ; Correlation analysis ; Cryopreservation ; Cryopreservation - methods ; Gene expression ; Gene Expression Regulation, Plant ; Genes ; Life Sciences ; Liquid nitrogen ; Membrane potential ; Membrane Potential, Mitochondrial ; Membranes ; Mitochondria ; Mortality ; Nitric oxide ; Nitric Oxide - metabolism ; Nitric Oxide Donors - pharmacology ; Nitroprusside - pharmacology ; Original Article ; Paeonia - cytology ; Paeonia - drug effects ; Paeonia - genetics ; Paeonia - metabolism ; Plant Biochemistry ; Plant Proteins - metabolism ; Plant Sciences ; Pollen ; Pollen - chemistry ; Pollen - cytology ; Pollen - genetics ; Pollen - metabolism ; Protease ; Single-nucleotide polymorphism ; Viability</subject><ispartof>Plant cell reports, 2021-12, Vol.40 (12), p.2383-2395</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021</rights><rights>2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.</rights><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-87c43769cee216af5e21a300e2938b9ac978cf9dacff8d41897af7fe5b345d6c3</citedby><cites>FETCH-LOGICAL-c375t-87c43769cee216af5e21a300e2938b9ac978cf9dacff8d41897af7fe5b345d6c3</cites><orcidid>0000-0001-5856-7665</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00299-021-02779-1$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00299-021-02779-1$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27915,27916,41479,42548,51310</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34459961$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ren, Ruifen</creatorcontrib><creatorcontrib>Zhou, Hao</creatorcontrib><creatorcontrib>Zhang, Lingling</creatorcontrib><creatorcontrib>Jiang, Xueru</creatorcontrib><creatorcontrib>Liu, Yan</creatorcontrib><title>Cryopreserved-pollen viability is regulated by NO-induced programmed cell death</title><title>Plant cell reports</title><addtitle>Plant Cell Rep</addtitle><addtitle>Plant Cell Rep</addtitle><description>Key message
After cryopreservation, the NO content in pollen increased, inducing programmed cell death as a key reason for reduced viability.
Low recovery of biomaterials after cryopreservation is a bottleneck that limits the application of this technology. At present, the mechanism of viability decline after cryopreservation is not fully understood. In this study, the effects of nitric oxide (NO) on programmed cell death (PCD) and its relationship with viability were investigated, using
Paeonia lactiflora
'Fen Yu Nu' pollen with significantly decreased viability after cryopreservation. The results showed that: the activity of caspase-3-like and caspase-9-like protease and the apoptosis rate of pollen cells were significantly increased, the expression level of the promoting PCD (pro-PCD) genes was up-regulated, while the expression level of the inhibiting PCD (anti-PCD) genes was down-regulated after preservation in liquid nitrogen (LN); the NO content in pollen cells increased significantly after LN exposure. The correlation analysis showed that NO was significantly correlated with pollen viability and all indicators of PCD. The addition of a NO carrier SNP after LN storage reduced pollen viability, increased endogenous NO content, decreased mitochondrial membrane potential level, activated caspase-3-like and caspase-9-like protease in pollen cells, and increased cell apoptosis rate. The expression levels of pro-PCD genes
PDCD2
and
ATG8CL
were significantly up-regulated, while the expression levels of anti-PCD genes
DAD1
,
BI-1
and
LSD1
were significantly down-regulated. The addition of NO scavenger c-PTIO improved pollen viability, and produced the opposite effect of sodium nitroferricyanide (III) dihydrate (SNP), but did not change the mitochondrial membrane potential. These results suggest that NO induced PCD during the cryopreservation of pollen, which was one of the reasons for the significant decrease of pollen viability after cryopreservation.</description><subject>Apoptosis</subject><subject>Apoptosis - genetics</subject><subject>Biomaterials</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedical materials</subject><subject>Biotechnology</subject><subject>Caspase-3</subject><subject>Caspase-9</subject><subject>Caspases - metabolism</subject><subject>Cell Biology</subject><subject>Cell death</subject><subject>Correlation analysis</subject><subject>Cryopreservation</subject><subject>Cryopreservation - methods</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Life Sciences</subject><subject>Liquid nitrogen</subject><subject>Membrane potential</subject><subject>Membrane Potential, Mitochondrial</subject><subject>Membranes</subject><subject>Mitochondria</subject><subject>Mortality</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - metabolism</subject><subject>Nitric Oxide Donors - pharmacology</subject><subject>Nitroprusside - pharmacology</subject><subject>Original Article</subject><subject>Paeonia - cytology</subject><subject>Paeonia - drug effects</subject><subject>Paeonia - genetics</subject><subject>Paeonia - metabolism</subject><subject>Plant Biochemistry</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Sciences</subject><subject>Pollen</subject><subject>Pollen - chemistry</subject><subject>Pollen - cytology</subject><subject>Pollen - genetics</subject><subject>Pollen - metabolism</subject><subject>Protease</subject><subject>Single-nucleotide polymorphism</subject><subject>Viability</subject><issn>0721-7714</issn><issn>1432-203X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kEtLxDAUhYMozjj6B1xIwY2bah5tHksZfMHgbBTchTS9HTv0MSbtQP-9GTsquHARbsL57snhIHRO8DXBWNx4jKlSMaYkHCFUTA7QlCSMxhSzt0M0xSJIQpBkgk68X2McRMGP0YQlSaoUJ1O0nLuh3Tjw4LaQx5u2qqCJtqXJyqrshqj0kYNVX5kO8igboudlXDZ5b8Nr49qVM3UdrhaqKsrBdO-n6KgwlYez_Zyh1_u7l_ljvFg-PM1vF7FlIu1iKewuirIAlHBTpGEYhjFQxWSmjFVC2kLlxhaFzBMilTCFKCDNWJLm3LIZuhp9Q4qPHnyn69LvYpgG2t5rmnJOOUkJC-jlH3Td9q4J6QKluCRMSBkoOlLWtd47KPTGlbVxgyZY7-rWY9061K2_6tYkLF3srfss9PCz8t1vANgI-CA1K3C_f_9j-wm4bYr9</recordid><startdate>20211201</startdate><enddate>20211201</enddate><creator>Ren, Ruifen</creator><creator>Zhou, Hao</creator><creator>Zhang, Lingling</creator><creator>Jiang, Xueru</creator><creator>Liu, Yan</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7T5</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5856-7665</orcidid></search><sort><creationdate>20211201</creationdate><title>Cryopreserved-pollen viability is regulated by NO-induced programmed cell death</title><author>Ren, Ruifen ; Zhou, Hao ; Zhang, Lingling ; Jiang, Xueru ; Liu, Yan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-87c43769cee216af5e21a300e2938b9ac978cf9dacff8d41897af7fe5b345d6c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Apoptosis</topic><topic>Apoptosis - genetics</topic><topic>Biomaterials</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedical materials</topic><topic>Biotechnology</topic><topic>Caspase-3</topic><topic>Caspase-9</topic><topic>Caspases - metabolism</topic><topic>Cell Biology</topic><topic>Cell death</topic><topic>Correlation analysis</topic><topic>Cryopreservation</topic><topic>Cryopreservation - methods</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Life Sciences</topic><topic>Liquid nitrogen</topic><topic>Membrane potential</topic><topic>Membrane Potential, Mitochondrial</topic><topic>Membranes</topic><topic>Mitochondria</topic><topic>Mortality</topic><topic>Nitric oxide</topic><topic>Nitric Oxide - metabolism</topic><topic>Nitric Oxide Donors - pharmacology</topic><topic>Nitroprusside - pharmacology</topic><topic>Original Article</topic><topic>Paeonia - cytology</topic><topic>Paeonia - drug effects</topic><topic>Paeonia - genetics</topic><topic>Paeonia - metabolism</topic><topic>Plant Biochemistry</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Sciences</topic><topic>Pollen</topic><topic>Pollen - chemistry</topic><topic>Pollen - cytology</topic><topic>Pollen - genetics</topic><topic>Pollen - metabolism</topic><topic>Protease</topic><topic>Single-nucleotide polymorphism</topic><topic>Viability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ren, Ruifen</creatorcontrib><creatorcontrib>Zhou, Hao</creatorcontrib><creatorcontrib>Zhang, Lingling</creatorcontrib><creatorcontrib>Jiang, Xueru</creatorcontrib><creatorcontrib>Liu, Yan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Plant cell reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ren, Ruifen</au><au>Zhou, Hao</au><au>Zhang, Lingling</au><au>Jiang, Xueru</au><au>Liu, Yan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cryopreserved-pollen viability is regulated by NO-induced programmed cell death</atitle><jtitle>Plant cell reports</jtitle><stitle>Plant Cell Rep</stitle><addtitle>Plant Cell Rep</addtitle><date>2021-12-01</date><risdate>2021</risdate><volume>40</volume><issue>12</issue><spage>2383</spage><epage>2395</epage><pages>2383-2395</pages><issn>0721-7714</issn><eissn>1432-203X</eissn><abstract>Key message
After cryopreservation, the NO content in pollen increased, inducing programmed cell death as a key reason for reduced viability.
Low recovery of biomaterials after cryopreservation is a bottleneck that limits the application of this technology. At present, the mechanism of viability decline after cryopreservation is not fully understood. In this study, the effects of nitric oxide (NO) on programmed cell death (PCD) and its relationship with viability were investigated, using
Paeonia lactiflora
'Fen Yu Nu' pollen with significantly decreased viability after cryopreservation. The results showed that: the activity of caspase-3-like and caspase-9-like protease and the apoptosis rate of pollen cells were significantly increased, the expression level of the promoting PCD (pro-PCD) genes was up-regulated, while the expression level of the inhibiting PCD (anti-PCD) genes was down-regulated after preservation in liquid nitrogen (LN); the NO content in pollen cells increased significantly after LN exposure. The correlation analysis showed that NO was significantly correlated with pollen viability and all indicators of PCD. The addition of a NO carrier SNP after LN storage reduced pollen viability, increased endogenous NO content, decreased mitochondrial membrane potential level, activated caspase-3-like and caspase-9-like protease in pollen cells, and increased cell apoptosis rate. The expression levels of pro-PCD genes
PDCD2
and
ATG8CL
were significantly up-regulated, while the expression levels of anti-PCD genes
DAD1
,
BI-1
and
LSD1
were significantly down-regulated. The addition of NO scavenger c-PTIO improved pollen viability, and produced the opposite effect of sodium nitroferricyanide (III) dihydrate (SNP), but did not change the mitochondrial membrane potential. These results suggest that NO induced PCD during the cryopreservation of pollen, which was one of the reasons for the significant decrease of pollen viability after cryopreservation.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>34459961</pmid><doi>10.1007/s00299-021-02779-1</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-5856-7665</orcidid></addata></record> |
| fulltext | fulltext |
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| ispartof | Plant cell reports, 2021-12, Vol.40 (12), p.2383-2395 |
| issn | 0721-7714 1432-203X |
| language | eng |
| recordid | cdi_proquest_miscellaneous_2566261513 |
| source | MEDLINE; Springer Nature - Complete Springer Journals |
| subjects | Apoptosis Apoptosis - genetics Biomaterials Biomedical and Life Sciences Biomedical materials Biotechnology Caspase-3 Caspase-9 Caspases - metabolism Cell Biology Cell death Correlation analysis Cryopreservation Cryopreservation - methods Gene expression Gene Expression Regulation, Plant Genes Life Sciences Liquid nitrogen Membrane potential Membrane Potential, Mitochondrial Membranes Mitochondria Mortality Nitric oxide Nitric Oxide - metabolism Nitric Oxide Donors - pharmacology Nitroprusside - pharmacology Original Article Paeonia - cytology Paeonia - drug effects Paeonia - genetics Paeonia - metabolism Plant Biochemistry Plant Proteins - metabolism Plant Sciences Pollen Pollen - chemistry Pollen - cytology Pollen - genetics Pollen - metabolism Protease Single-nucleotide polymorphism Viability |
| title | Cryopreserved-pollen viability is regulated by NO-induced programmed cell death |
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