Programmed Cell Death Progresses Differentially in Epidermal and Mesophyll Cells of Lily Petals
In the petals of some species of flowers, programmed cell death (PCD) begins earlier in mesophyll cells than in epidermal cells. However, PCD progression in each cell type has not been characterized in detail. We separately constructed a time course of biochemical signs and expression patterns of PC...
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| creator | Mochizuki-Kawai, Hiroko Niki, Tomoko Shibuya, Kenichi Ichimura, Kazuo |
| description | In the petals of some species of flowers, programmed cell death (PCD) begins earlier in mesophyll cells than in epidermal cells. However, PCD progression in each cell type has not been characterized in detail. We separately constructed a time course of biochemical signs and expression patterns of PCD-associated genes in epidermal and mesophyll cells in Lilium cv. Yelloween petals. Before visible signs of senescence could be observed, we found signs of PCD, including DNA degradation and decreased protein content in mesophyll cells only. In these cells, the total proteinase activity increased on the day after anthesis. Within 3 days after anthesis, the protein content decreased by 61.8%, and 22.8% of mesophyll cells was lost. A second peak of proteinase activity was observed on day 6, and the number of mesophyll cells decreased again from days 4 to 7. These biochemical and morphological results suggest that PCD progressed in steps during flower life in the mesophyll cells. PCD began in epidermal cells on day 5, in temporal synchrony with the time course of visible senescence. In the mesophyll cells, the KDEL-tailed cysteine proteinase (LoCYP) and S1/P1 nuclease (LoNUC) genes were upregulated before petal wilting, earlier than in epidermal cells. In contrast, relative to that in the mesophyll cells, the expression of the SAG12 cysteine proteinase homolog (LoSAG12) drastically increased in epidermal cells in the final stage of senescence. These results suggest that multiple PCD-associated genes differentially contribute to the time lag of PCD progression between epidermal and mesophyll cells of lily petals. |
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However, PCD progression in each cell type has not been characterized in detail. We separately constructed a time course of biochemical signs and expression patterns of PCD-associated genes in epidermal and mesophyll cells in Lilium cv. Yelloween petals. Before visible signs of senescence could be observed, we found signs of PCD, including DNA degradation and decreased protein content in mesophyll cells only. In these cells, the total proteinase activity increased on the day after anthesis. Within 3 days after anthesis, the protein content decreased by 61.8%, and 22.8% of mesophyll cells was lost. A second peak of proteinase activity was observed on day 6, and the number of mesophyll cells decreased again from days 4 to 7. These biochemical and morphological results suggest that PCD progressed in steps during flower life in the mesophyll cells. PCD began in epidermal cells on day 5, in temporal synchrony with the time course of visible senescence. In the mesophyll cells, the KDEL-tailed cysteine proteinase (LoCYP) and S1/P1 nuclease (LoNUC) genes were upregulated before petal wilting, earlier than in epidermal cells. In contrast, relative to that in the mesophyll cells, the expression of the SAG12 cysteine proteinase homolog (LoSAG12) drastically increased in epidermal cells in the final stage of senescence. These results suggest that multiple PCD-associated genes differentially contribute to the time lag of PCD progression between epidermal and mesophyll cells of lily petals.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0143502</identifier><identifier>PMID: 26605547</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aging - genetics ; Alstroemeria ; Apoptosis ; Apoptosis - genetics ; Arabidopsis ; Biochemistry ; Cell death ; Cell Survival - genetics ; Cysteine ; Cysteine proteinase ; Deoxyribonucleic acid ; Dianthus caryophyllus ; DNA ; DNA Fragmentation ; Enzymes ; Flowers ; Flowers & plants ; Flowers - genetics ; Gene expression ; Gene Expression Regulation, Plant ; Genes ; Hemerocallis ; Homology ; Ipomoea nil ; Lilium ; Lilium - genetics ; Lilium - metabolism ; Lilium longiflorum ; Mesophyll ; Mesophyll Cells - metabolism ; Nitrogen - metabolism ; Nuclease ; Peptide Hydrolases - metabolism ; Petals ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Proteinase ; Risk factors ; Seeds ; Senescence ; Time lag ; Wilting</subject><ispartof>PloS one, 2015-11, Vol.10 (11), p.e0143502-e0143502</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Mochizuki-Kawai et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Mochizuki-Kawai et al 2015 Mochizuki-Kawai et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-ba1b94de0511897461f8f065e182be2537ced69469ebb5ead631648fc060d5623</citedby><cites>FETCH-LOGICAL-c692t-ba1b94de0511897461f8f065e182be2537ced69469ebb5ead631648fc060d5623</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4659684/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4659684/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23871,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26605547$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Kalaitzis, Panagiotis</contributor><creatorcontrib>Mochizuki-Kawai, Hiroko</creatorcontrib><creatorcontrib>Niki, Tomoko</creatorcontrib><creatorcontrib>Shibuya, Kenichi</creatorcontrib><creatorcontrib>Ichimura, Kazuo</creatorcontrib><title>Programmed Cell Death Progresses Differentially in Epidermal and Mesophyll Cells of Lily Petals</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In the petals of some species of flowers, programmed cell death (PCD) begins earlier in mesophyll cells than in epidermal cells. However, PCD progression in each cell type has not been characterized in detail. We separately constructed a time course of biochemical signs and expression patterns of PCD-associated genes in epidermal and mesophyll cells in Lilium cv. Yelloween petals. Before visible signs of senescence could be observed, we found signs of PCD, including DNA degradation and decreased protein content in mesophyll cells only. In these cells, the total proteinase activity increased on the day after anthesis. Within 3 days after anthesis, the protein content decreased by 61.8%, and 22.8% of mesophyll cells was lost. A second peak of proteinase activity was observed on day 6, and the number of mesophyll cells decreased again from days 4 to 7. These biochemical and morphological results suggest that PCD progressed in steps during flower life in the mesophyll cells. PCD began in epidermal cells on day 5, in temporal synchrony with the time course of visible senescence. In the mesophyll cells, the KDEL-tailed cysteine proteinase (LoCYP) and S1/P1 nuclease (LoNUC) genes were upregulated before petal wilting, earlier than in epidermal cells. In contrast, relative to that in the mesophyll cells, the expression of the SAG12 cysteine proteinase homolog (LoSAG12) drastically increased in epidermal cells in the final stage of senescence. These results suggest that multiple PCD-associated genes differentially contribute to the time lag of PCD progression between epidermal and mesophyll cells of lily petals.</description><subject>Aging - genetics</subject><subject>Alstroemeria</subject><subject>Apoptosis</subject><subject>Apoptosis - genetics</subject><subject>Arabidopsis</subject><subject>Biochemistry</subject><subject>Cell death</subject><subject>Cell Survival - genetics</subject><subject>Cysteine</subject><subject>Cysteine proteinase</subject><subject>Deoxyribonucleic acid</subject><subject>Dianthus caryophyllus</subject><subject>DNA</subject><subject>DNA Fragmentation</subject><subject>Enzymes</subject><subject>Flowers</subject><subject>Flowers & plants</subject><subject>Flowers - genetics</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Hemerocallis</subject><subject>Homology</subject><subject>Ipomoea nil</subject><subject>Lilium</subject><subject>Lilium - genetics</subject><subject>Lilium - metabolism</subject><subject>Lilium longiflorum</subject><subject>Mesophyll</subject><subject>Mesophyll Cells - metabolism</subject><subject>Nitrogen - metabolism</subject><subject>Nuclease</subject><subject>Peptide Hydrolases - metabolism</subject><subject>Petals</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Proteinase</subject><subject>Risk factors</subject><subject>Seeds</subject><subject>Senescence</subject><subject>Time lag</subject><subject>Wilting</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</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><sourceid>DOA</sourceid><recordid>eNqNk19v0zAUxSMEYmPwDRBEQkLw0GLHjuO8IE3dgEpFm_j3ajnxdevKiTs7mdZvj9tmU4P2gPLg6OZ3jn1PrpPkNUZTTAr8ae1630o73bgWpghTkqPsSXKKS5JNWIbI06P3k-RFCGuEcsIZe56cZIyhPKfFaSKuvVt62TSg0hlYm16A7FbpvgohQEgvjNbgoe2MtHabmja93BgFvpE2la1Kv0Nwm9U2Snf6kDqdLkwEr6GTNrxMnum4wKthPUt-f7n8Nfs2WVx9nc_OF5OalVk3qSSuSqoA5RjzsqAMa64RywHzrIIsJ0UNipWUlVBVOUjFCGaU6xoxpHKWkbPk7cF3Y10QQzZB4IIwijjOeCTmB0I5uRYbbxrpt8JJI_YF55dC-s7UFgSWlQINijJCaZRXVTwRKVilZYmLDEevz8NufRWTq2M6XtqR6fhLa1Zi6W4FZXnJOI0GHwYD7256CJ1oTKhjfrIF1-_PzSnHmOw6e_cP-nh3A7WUsQHTahf3rXem4jyOBkOY0zJS00eo-ChoTB0HSZtYHwk-jgSR6eCuW8o-BDH_-eP_2as_Y_b9EbsCabtVcLbvjGvDGKQHsPYuBA_6IWSMxO4e3KchdvdADPcgyt4c_6AH0f3gk7936QGk</recordid><startdate>20151125</startdate><enddate>20151125</enddate><creator>Mochizuki-Kawai, Hiroko</creator><creator>Niki, Tomoko</creator><creator>Shibuya, Kenichi</creator><creator>Ichimura, Kazuo</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151125</creationdate><title>Programmed Cell Death Progresses Differentially in Epidermal and Mesophyll Cells of Lily Petals</title><author>Mochizuki-Kawai, Hiroko ; Niki, Tomoko ; Shibuya, Kenichi ; Ichimura, Kazuo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-ba1b94de0511897461f8f065e182be2537ced69469ebb5ead631648fc060d5623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Aging - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mochizuki-Kawai, Hiroko</au><au>Niki, Tomoko</au><au>Shibuya, Kenichi</au><au>Ichimura, Kazuo</au><au>Kalaitzis, Panagiotis</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Programmed Cell Death Progresses Differentially in Epidermal and Mesophyll Cells of Lily Petals</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-11-25</date><risdate>2015</risdate><volume>10</volume><issue>11</issue><spage>e0143502</spage><epage>e0143502</epage><pages>e0143502-e0143502</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In the petals of some species of flowers, programmed cell death (PCD) begins earlier in mesophyll cells than in epidermal cells. However, PCD progression in each cell type has not been characterized in detail. We separately constructed a time course of biochemical signs and expression patterns of PCD-associated genes in epidermal and mesophyll cells in Lilium cv. Yelloween petals. Before visible signs of senescence could be observed, we found signs of PCD, including DNA degradation and decreased protein content in mesophyll cells only. In these cells, the total proteinase activity increased on the day after anthesis. Within 3 days after anthesis, the protein content decreased by 61.8%, and 22.8% of mesophyll cells was lost. A second peak of proteinase activity was observed on day 6, and the number of mesophyll cells decreased again from days 4 to 7. These biochemical and morphological results suggest that PCD progressed in steps during flower life in the mesophyll cells. PCD began in epidermal cells on day 5, in temporal synchrony with the time course of visible senescence. In the mesophyll cells, the KDEL-tailed cysteine proteinase (LoCYP) and S1/P1 nuclease (LoNUC) genes were upregulated before petal wilting, earlier than in epidermal cells. In contrast, relative to that in the mesophyll cells, the expression of the SAG12 cysteine proteinase homolog (LoSAG12) drastically increased in epidermal cells in the final stage of senescence. These results suggest that multiple PCD-associated genes differentially contribute to the time lag of PCD progression between epidermal and mesophyll cells of lily petals.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26605547</pmid><doi>10.1371/journal.pone.0143502</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Aging - genetics Alstroemeria Apoptosis Apoptosis - genetics Arabidopsis Biochemistry Cell death Cell Survival - genetics Cysteine Cysteine proteinase Deoxyribonucleic acid Dianthus caryophyllus DNA DNA Fragmentation Enzymes Flowers Flowers & plants Flowers - genetics Gene expression Gene Expression Regulation, Plant Genes Hemerocallis Homology Ipomoea nil Lilium Lilium - genetics Lilium - metabolism Lilium longiflorum Mesophyll Mesophyll Cells - metabolism Nitrogen - metabolism Nuclease Peptide Hydrolases - metabolism Petals Plant Proteins - genetics Plant Proteins - metabolism Proteinase Risk factors Seeds Senescence Time lag Wilting |
| title | Programmed Cell Death Progresses Differentially in Epidermal and Mesophyll Cells of Lily Petals |
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