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Programmed Cell Death in Plants

Year 2021, , 1700 - 1712, 01.09.2021
https://doi.org/10.21597/jist.800066

Abstract

Organisms are born, grow, reproduce and die throughout their basic life cycle. Homeostasis (maintenance of internal balance) in multicellular organisms in these process is achieved by maintaining the balance between cell proliferation and programmed cell death. Controlled disintegration of aged, completed, or damaged tissues by organism due to various reasons such as the formation of tracheal elements, leaf senescence or resistance to stress factors is realized with the help of programmed cell death (PCD). This process controlled by a variety of environmental factors is also directed by molecularly. Programmed cell death types identified in animals are explained in detail. As well as the types of programmed cell death in plants have not been completely clarified, it has recently collected under two main topics as developmentally related programmed cell death (dPCD) and environmentally induced cell death (ePCD). In this review, the types of programmed cell death in plants are described and explained with their examples.

References

  • Balakireva AV, Zamyatnin Jr. A, 2019. Cutting Out the Gaps Between Proteases and Programmed Cell Death. Frontiers in Plant Science, 10: 704.
  • Bertoni G, 2016. What the Nucellus Can Tell Us. The Plant Cell, 28 (6): 1234.
  • Bozhkov PV, 2018. Plant autophagy: mechanisms and functions. Journal of Experimental Botany, 69 (6): 1281–1285.
  • Buono RA, Hudecek R, Nowack MK, 2019. Plant proteases during developmental programmed cell death. Journal of Experimental Botany, 70 (7): 2097-2112.
  • Büyükkartal N, 2000. Bitki Embriyolojisi Laboratuvar Kılavuzu. A.Ü.F.F Döner Sermaye İşletmesi Yayınları, Ankara-Türkiye.
  • Conway TC, McCabe PF, 2018. Plant Programmed Cell Death (PCD): Using Cell Morphology as a Tool to Investigate Plant PCD. Springer International Publishing, pp.273-281, Cham-Switzerland.
  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K, 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology, 11: 163-177.
  • Daneva A, Gao Z, Durme MV, Nowack MK, 2016. Functions and Regulation of Programmed Cell Death in Plant Development. Annual Review of Cell Developmental Biology, 32: 441-468.
  • Dauphinee AN, Gunawardena AN, 2015. An Overview of Programmed Cell Death Research: From Canonical to Emerging Model Species. Springer International Publishing, pp. 1-32, Switzerland.
  • Dickman M, Williams B, Li Y, Figueiredo P, Wolpert T, 2017. Reassessing apoptosis in plants. Nature Plants, 3 (10): 773-779.
  • Dominguez F, Cejudo FJ, 2014. Programmed cell death (PCD): an essential process of cereal seed development and germination. Frontiers in Plant Science, 5: 366.
  • Eckardt NA, 2007. Elucidating the Function of Synergid Cells: A Regulatory Role for MYB98. The Plant Cell, 19: 2320–2321.
  • Fendrych M, Van Hautegem T, Van Durme M, Olvera-Carrillo Y, Huysmans M, Karimi M, Lippens S, Guérin CJ, Krebs M, Schumacher, K, Nowack MK, 2014. Programmed Cell Death Controlled by ANAC033/SOMBRERO Determines Root Cap Organ Size in Arabidopsis. Current Biology, 24 (9): 931-940.
  • Greenberg JT, 1996. Programmed cell death: A way of life for plants. Proceedings of the National Academy of Sciences, 93 (22): 12094-12097.
  • Gunawardena AHLAN, 2008. Programmed Cell Death and Tissue Remodelling in Plants. Journal of Experimental Botany, 59 (3): 445-451.
  • Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE, 2001. Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta, 212: 205-214.
  • Gunawardena AHLAN, Sault K, Donnelly P, Greenwood JS, Dengler NG, 2005. Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae). Planta, 221 (5): 607-618.
  • Hautegem TV, Waters AJ, Goodrich J, Nowack MK, 2015. Only in dying, life: programmed cell death during plant development. Trends in Plant Science, 20 (2): 102-113.
  • Heath MC, 2000. Hypersensitive response-related death. Plant Molecular Biology, 44: 321-334.
  • Huysmans M, Lema S, Coll NS, Nowack MK, 2017. Dying two deaths — programmed cell death regulationin development and disease. Current Opinion in Plant Biology, 35: 37-44.
  • Kacprzyk J, Dauphinee AN, Gallois P, Gunawardena AHLAN, McCabe PF, 2016. Methods of Study Plant Programmed Cell Death. Humana Press pp. 145-160, New York.
  • Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K, 2006. Abolition of the Tapetum Suicide Program Ruins Microsporogenesis. Plant Cell Physiology, 47 (6): 784–787.
  • Ke S, Liu S, Luan X, Xie XM, Hsieh TF, Zhang XQ, 2019. Mutation in a Putative Glycosyltransferaselike Gene Causes Programmed Cell Death and Early Leaf Senescence in Rice. Rice, 12:7.
  • Korkmaz Ş, Ak BE, Sakar E, Turanoğlu İ, Söylemez S, 2015. Meyve Ağaçlarında Uyuşmazlık ve Mekanizması. Harran Tarım ve Gıda Bilimleri Dergisi, 19: 180-186.
  • Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny, MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death and Differentiation, 16: 3–11.
  • Kwon SI, Park OK, 2008. Autophagy in Plants. Journal of Plant Biology, 51: 313-320.
  • Lam E, 2004. Controlled cell death,plant survıval and development. Nature Reviews Molecular Cell Biology, 5 (4): 305-315.
  • Lim PO, Kim HJ, Nam HG, 2007. Leaf senesence. Annual Review of Plant Biology, 58: 115-136.
  • Lima NB, Trindade FG, Cunha M, Oliveira AEA, Topping J, Lindsey K, Fernandes KVS, 2015. Programmed cell death during development of cowpea (Vigna unguiculata (L.) Walp.) seed coat. Plant, Cell and Environment, 38: 718-728.
  • Lincoln JE, Sanchez JP, Zumstein K, Gilchrist DG, 2018. Plant and animal PR1 family members inhibit programmed cell death and suppress bacterial pathogens in plant tissues. Molecular Plant Pathology, 19: 2111-2123.
  • Locato V, De Gara L, 2018. Programmed Cell Death in Plants: An Overview. Humana press, pp. 1-8, New York. Ma N, Ma C, Liu Y, Shahdid M, Wang C, Gao J, 2018. Petal senesence:a hormone view. Journal of Experimental Botany, 69 (4): 719-732.
  • Matilla AJ, 2019. Programmed Cell Death in Seeds: An Adaptive Mechanism Required for Life [Online First]. IntechOpen, DOI: 10.5772/intechopen.86833.
  • Minina EA, Smertenko AP, Bozhlov PV, 2014. Vacuolar cell death in plants. Autophagy, 10 (5): 928-929. Munné-Bosch S, 2016. Flower senescence and other programmed cell death processes in plants: a tribute to the late Wouter G. van Doorn. Journal of Experimental Botany, 67 (20): 5885–5886.
  • Palavan-Ünsal N, Büyüktuncer ED, Tüfekçi MA, 2005. Programmed cell death in plants. Journal of Cell and Molecular Biology, 4: 9-23.
  • Radchuk V, Borisjuk L, 2014. Physical, metabolic and developmental functions of the seed coat. Frontiers in Plant Science, 5: 510.
  • Reape TJ, Molony EM, McCabe PF, 2008. Programmed cell death in plants: distinguishing between different modes. Journal of Experimental Botany, 59 (3): 435–444.
  • Rogers H, Munne-Bosch S, 2016. Production and Scavenging of Reactive Oxygen Species and Redox Signaling during Leaf and Flower Senescence: Similar But Different. Plant Phsiology, 171: 1560-1568.
  • Schwartz BW, Vernon DM, Meinke DW, 1997. Development of the Suspensor: Differentiation, Communication and Programmed Cell Death During Plant Embryogenesis. Kuluver Academic Publishers, pp. 53-72, USA. Shibuya K, Yamada T, Ichimura K, 2016. Morphological changes in senescing petal cells and the regulatory mechanism of petal senescence. Journal of Experimental Botany, 67 (20): 5909-5918.
  • Toker MC, 2004. Bitki Morfolojisi. Ankara Üniversitesi Fen Fakültesi Biyoloji Bölümü Yayınları No:2, ss. 100-102, Ankara.
  • Van Doorn WG, 2005. Plant Programmed cell death and the point of no return. TRENDS in plant science, 10 (10): 478-483.
  • Van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LAJ, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV, 2011. Morphological classification of plant cell deaths. Cell Death and Differentiation, 18(8): 1241-1246.
  • Van Doorn WG, Woltering, EJ, 2005. Many ways to exit? Cell death categories in plants. TRENDS in Plant Science, 10 (3): 117-122.
  • Vardar F, Ünal M, 2011. Cytochemical and ultrastructural observations of anthers and pollen grains in Lathyrus undulatus Boiss. Acta Botanica Croatica, 70 (1), 53-64.
  • Vardar F, Ünal M, 2012. Ultrastructural aspects and programmed cell death in the tapetal cells of Lathyrus undulatus Boiss. Acta Biologica Hungarica, 63 (1), 52–66.
  • Vianello A, Zancani M, Peresson C, Petrussa E, Casolo V, Krajnakova J, Patui S, Braidot E, Macri F, 2007. Plant mitochondrial pathway leading to programmed cell death. Physiologia Plantarum, 129: 242–252.
  • Wertman J, Lord CE, Dauphinee AN, Gunawardena AH, 2012. The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biology, 12: 115-131.
  • Xu Y, Hanson MR, 2000. Programmed Cell Death during Pollination-Induced Petal Senescence in Petunia. Plant PhySiology, 122: 1323–1333.
  • Yoshida S, 2003. Molecular regulation on leaf senesence. Current Opinion in Plant Biology, 6: 79-84.

Bitkilerde Programlı Hücre Ölümü

Year 2021, , 1700 - 1712, 01.09.2021
https://doi.org/10.21597/jist.800066

Abstract

Canlılar; temel yaşam döngüleri boyunca doğar, büyür, çoğalır ve ölürler. Çok hücreli organizmalarda
bu süreç içerisinde homeostazi (iç dengenin korunması); hücre çoğalması ve programlı hücre ölümü arasındaki dengenin devamlılığı ile sağlanmaktadır. Trakeal elementlerin oluşumu, yaprak senesensi ya da stres faktörlerine dayanıklılık gibi çeşitli nedenlerden dolayı yaşlanmış, görevini tamamlamış ya da hasar görmüş dokuların organizma tarafından kontrollü olarak parçalanması “programlı hücre ölümü (PCD)” yardımı ile gerçekleşmektedir. Çeşitli çevresel etmenler tarafından kontrol edilen bu süreç, aynı zamanda moleküler olarak da yönlendirilmektedir. Hayvanlarda belirlenen programlı hücre ölümü tipleri oldukça detaylı açıklanmıştır. Bitkilerde görülen programlı hücre ölümü tipleri ise tam olarak aydınlatılamamış olmakla birlikte; son zamanlarda gelişimsel olarak düzenlenmiş hücre ölümü (dPCD) ve çevre tarafından indüklenmiş hücre ölümü (ePCD) olarak iki ana başlık altında toplanmıştır. Gerçekleştirilen bu derlemede bitkilerde görülen programlı hücre ölümü tipleri tanımlanarak örnekleriyle birlikte açıklanmaya çalışılmıştır.

References

  • Balakireva AV, Zamyatnin Jr. A, 2019. Cutting Out the Gaps Between Proteases and Programmed Cell Death. Frontiers in Plant Science, 10: 704.
  • Bertoni G, 2016. What the Nucellus Can Tell Us. The Plant Cell, 28 (6): 1234.
  • Bozhkov PV, 2018. Plant autophagy: mechanisms and functions. Journal of Experimental Botany, 69 (6): 1281–1285.
  • Buono RA, Hudecek R, Nowack MK, 2019. Plant proteases during developmental programmed cell death. Journal of Experimental Botany, 70 (7): 2097-2112.
  • Büyükkartal N, 2000. Bitki Embriyolojisi Laboratuvar Kılavuzu. A.Ü.F.F Döner Sermaye İşletmesi Yayınları, Ankara-Türkiye.
  • Conway TC, McCabe PF, 2018. Plant Programmed Cell Death (PCD): Using Cell Morphology as a Tool to Investigate Plant PCD. Springer International Publishing, pp.273-281, Cham-Switzerland.
  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K, 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology, 11: 163-177.
  • Daneva A, Gao Z, Durme MV, Nowack MK, 2016. Functions and Regulation of Programmed Cell Death in Plant Development. Annual Review of Cell Developmental Biology, 32: 441-468.
  • Dauphinee AN, Gunawardena AN, 2015. An Overview of Programmed Cell Death Research: From Canonical to Emerging Model Species. Springer International Publishing, pp. 1-32, Switzerland.
  • Dickman M, Williams B, Li Y, Figueiredo P, Wolpert T, 2017. Reassessing apoptosis in plants. Nature Plants, 3 (10): 773-779.
  • Dominguez F, Cejudo FJ, 2014. Programmed cell death (PCD): an essential process of cereal seed development and germination. Frontiers in Plant Science, 5: 366.
  • Eckardt NA, 2007. Elucidating the Function of Synergid Cells: A Regulatory Role for MYB98. The Plant Cell, 19: 2320–2321.
  • Fendrych M, Van Hautegem T, Van Durme M, Olvera-Carrillo Y, Huysmans M, Karimi M, Lippens S, Guérin CJ, Krebs M, Schumacher, K, Nowack MK, 2014. Programmed Cell Death Controlled by ANAC033/SOMBRERO Determines Root Cap Organ Size in Arabidopsis. Current Biology, 24 (9): 931-940.
  • Greenberg JT, 1996. Programmed cell death: A way of life for plants. Proceedings of the National Academy of Sciences, 93 (22): 12094-12097.
  • Gunawardena AHLAN, 2008. Programmed Cell Death and Tissue Remodelling in Plants. Journal of Experimental Botany, 59 (3): 445-451.
  • Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE, 2001. Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta, 212: 205-214.
  • Gunawardena AHLAN, Sault K, Donnelly P, Greenwood JS, Dengler NG, 2005. Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae). Planta, 221 (5): 607-618.
  • Hautegem TV, Waters AJ, Goodrich J, Nowack MK, 2015. Only in dying, life: programmed cell death during plant development. Trends in Plant Science, 20 (2): 102-113.
  • Heath MC, 2000. Hypersensitive response-related death. Plant Molecular Biology, 44: 321-334.
  • Huysmans M, Lema S, Coll NS, Nowack MK, 2017. Dying two deaths — programmed cell death regulationin development and disease. Current Opinion in Plant Biology, 35: 37-44.
  • Kacprzyk J, Dauphinee AN, Gallois P, Gunawardena AHLAN, McCabe PF, 2016. Methods of Study Plant Programmed Cell Death. Humana Press pp. 145-160, New York.
  • Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K, 2006. Abolition of the Tapetum Suicide Program Ruins Microsporogenesis. Plant Cell Physiology, 47 (6): 784–787.
  • Ke S, Liu S, Luan X, Xie XM, Hsieh TF, Zhang XQ, 2019. Mutation in a Putative Glycosyltransferaselike Gene Causes Programmed Cell Death and Early Leaf Senescence in Rice. Rice, 12:7.
  • Korkmaz Ş, Ak BE, Sakar E, Turanoğlu İ, Söylemez S, 2015. Meyve Ağaçlarında Uyuşmazlık ve Mekanizması. Harran Tarım ve Gıda Bilimleri Dergisi, 19: 180-186.
  • Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny, MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death and Differentiation, 16: 3–11.
  • Kwon SI, Park OK, 2008. Autophagy in Plants. Journal of Plant Biology, 51: 313-320.
  • Lam E, 2004. Controlled cell death,plant survıval and development. Nature Reviews Molecular Cell Biology, 5 (4): 305-315.
  • Lim PO, Kim HJ, Nam HG, 2007. Leaf senesence. Annual Review of Plant Biology, 58: 115-136.
  • Lima NB, Trindade FG, Cunha M, Oliveira AEA, Topping J, Lindsey K, Fernandes KVS, 2015. Programmed cell death during development of cowpea (Vigna unguiculata (L.) Walp.) seed coat. Plant, Cell and Environment, 38: 718-728.
  • Lincoln JE, Sanchez JP, Zumstein K, Gilchrist DG, 2018. Plant and animal PR1 family members inhibit programmed cell death and suppress bacterial pathogens in plant tissues. Molecular Plant Pathology, 19: 2111-2123.
  • Locato V, De Gara L, 2018. Programmed Cell Death in Plants: An Overview. Humana press, pp. 1-8, New York. Ma N, Ma C, Liu Y, Shahdid M, Wang C, Gao J, 2018. Petal senesence:a hormone view. Journal of Experimental Botany, 69 (4): 719-732.
  • Matilla AJ, 2019. Programmed Cell Death in Seeds: An Adaptive Mechanism Required for Life [Online First]. IntechOpen, DOI: 10.5772/intechopen.86833.
  • Minina EA, Smertenko AP, Bozhlov PV, 2014. Vacuolar cell death in plants. Autophagy, 10 (5): 928-929. Munné-Bosch S, 2016. Flower senescence and other programmed cell death processes in plants: a tribute to the late Wouter G. van Doorn. Journal of Experimental Botany, 67 (20): 5885–5886.
  • Palavan-Ünsal N, Büyüktuncer ED, Tüfekçi MA, 2005. Programmed cell death in plants. Journal of Cell and Molecular Biology, 4: 9-23.
  • Radchuk V, Borisjuk L, 2014. Physical, metabolic and developmental functions of the seed coat. Frontiers in Plant Science, 5: 510.
  • Reape TJ, Molony EM, McCabe PF, 2008. Programmed cell death in plants: distinguishing between different modes. Journal of Experimental Botany, 59 (3): 435–444.
  • Rogers H, Munne-Bosch S, 2016. Production and Scavenging of Reactive Oxygen Species and Redox Signaling during Leaf and Flower Senescence: Similar But Different. Plant Phsiology, 171: 1560-1568.
  • Schwartz BW, Vernon DM, Meinke DW, 1997. Development of the Suspensor: Differentiation, Communication and Programmed Cell Death During Plant Embryogenesis. Kuluver Academic Publishers, pp. 53-72, USA. Shibuya K, Yamada T, Ichimura K, 2016. Morphological changes in senescing petal cells and the regulatory mechanism of petal senescence. Journal of Experimental Botany, 67 (20): 5909-5918.
  • Toker MC, 2004. Bitki Morfolojisi. Ankara Üniversitesi Fen Fakültesi Biyoloji Bölümü Yayınları No:2, ss. 100-102, Ankara.
  • Van Doorn WG, 2005. Plant Programmed cell death and the point of no return. TRENDS in plant science, 10 (10): 478-483.
  • Van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LAJ, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV, 2011. Morphological classification of plant cell deaths. Cell Death and Differentiation, 18(8): 1241-1246.
  • Van Doorn WG, Woltering, EJ, 2005. Many ways to exit? Cell death categories in plants. TRENDS in Plant Science, 10 (3): 117-122.
  • Vardar F, Ünal M, 2011. Cytochemical and ultrastructural observations of anthers and pollen grains in Lathyrus undulatus Boiss. Acta Botanica Croatica, 70 (1), 53-64.
  • Vardar F, Ünal M, 2012. Ultrastructural aspects and programmed cell death in the tapetal cells of Lathyrus undulatus Boiss. Acta Biologica Hungarica, 63 (1), 52–66.
  • Vianello A, Zancani M, Peresson C, Petrussa E, Casolo V, Krajnakova J, Patui S, Braidot E, Macri F, 2007. Plant mitochondrial pathway leading to programmed cell death. Physiologia Plantarum, 129: 242–252.
  • Wertman J, Lord CE, Dauphinee AN, Gunawardena AH, 2012. The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biology, 12: 115-131.
  • Xu Y, Hanson MR, 2000. Programmed Cell Death during Pollination-Induced Petal Senescence in Petunia. Plant PhySiology, 122: 1323–1333.
  • Yoshida S, 2003. Molecular regulation on leaf senesence. Current Opinion in Plant Biology, 6: 79-84.
There are 48 citations in total.

Details

Primary Language Turkish
Subjects Structural Biology
Journal Section Bitki Fizyolojisi / Plant Physiology
Authors

Halide Hande Güngör 0000-0003-4155-4926

Begüm Güler 0000-0002-9970-2111

Meltem Bayraktar 0000-0002-7569-6925

Aynur Gürel 0000-0002-7002-9752

Publication Date September 1, 2021
Submission Date September 25, 2020
Acceptance Date April 1, 2021
Published in Issue Year 2021

Cite

APA Güngör, H. H., Güler, B., Bayraktar, M., Gürel, A. (2021). Bitkilerde Programlı Hücre Ölümü. Journal of the Institute of Science and Technology, 11(3), 1700-1712. https://doi.org/10.21597/jist.800066
AMA Güngör HH, Güler B, Bayraktar M, Gürel A. Bitkilerde Programlı Hücre Ölümü. Iğdır Üniv. Fen Bil Enst. Der. September 2021;11(3):1700-1712. doi:10.21597/jist.800066
Chicago Güngör, Halide Hande, Begüm Güler, Meltem Bayraktar, and Aynur Gürel. “Bitkilerde Programlı Hücre Ölümü”. Journal of the Institute of Science and Technology 11, no. 3 (September 2021): 1700-1712. https://doi.org/10.21597/jist.800066.
EndNote Güngör HH, Güler B, Bayraktar M, Gürel A (September 1, 2021) Bitkilerde Programlı Hücre Ölümü. Journal of the Institute of Science and Technology 11 3 1700–1712.
IEEE H. H. Güngör, B. Güler, M. Bayraktar, and A. Gürel, “Bitkilerde Programlı Hücre Ölümü”, Iğdır Üniv. Fen Bil Enst. Der., vol. 11, no. 3, pp. 1700–1712, 2021, doi: 10.21597/jist.800066.
ISNAD Güngör, Halide Hande et al. “Bitkilerde Programlı Hücre Ölümü”. Journal of the Institute of Science and Technology 11/3 (September 2021), 1700-1712. https://doi.org/10.21597/jist.800066.
JAMA Güngör HH, Güler B, Bayraktar M, Gürel A. Bitkilerde Programlı Hücre Ölümü. Iğdır Üniv. Fen Bil Enst. Der. 2021;11:1700–1712.
MLA Güngör, Halide Hande et al. “Bitkilerde Programlı Hücre Ölümü”. Journal of the Institute of Science and Technology, vol. 11, no. 3, 2021, pp. 1700-12, doi:10.21597/jist.800066.
Vancouver Güngör HH, Güler B, Bayraktar M, Gürel A. Bitkilerde Programlı Hücre Ölümü. Iğdır Üniv. Fen Bil Enst. Der. 2021;11(3):1700-12.