Autophagy is associated with male sterility in pistillate flowers of Maytenus obtusifolia (Celastraceae)
Isabella Veríssimo Nader Haddad A C , Lygia Dolores Ribeiro de Santiago-Fernandes A and Silvia Rodrigues Machado B
+ Author Affiliations
- Author Affiliations
A Departamento de Botânica, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, Rio de Janeiro, RJ 22940-040, Brazil.
B Departamento de Botânica, Instituto de Biociências, Universidade Estadual Paulista, Caixa Postal 510, Botucatu, SP 18618-000, Brazil.
C Corresponding author. Email: isabellahaddad@gmail.com
Australian Journal of Botany 66(2) 108-115 https://doi.org/10.1071/BT17174
Submitted: 19 September 2017 Accepted: 12 January 2018 Published: 19 February 2018
Abstract
Programmed cell death (PCD) is defined as a sequence of genetically regulated events leading to controlled and organised cellular degradation. It plays a vital role in plant development; however, little is known about the role of PCD in reproductive development. Sterility in pistillate flowers of Maytenus obtusifolia Mart. has been shown to be related to cytoplasmic male sterility (CMS) based on reproductive biology and anatomical analysis. The recurrent PCD led us to investigate changes in the tapetum and sporogenic tissue during the establishment of male sterility using light and transmission electron microscopy combined with the use of TUNEL (terminal deoxynucleotidyl transferase mediated dUDP end-labelling) assay. The interruption of pollen development in pistillate flowers is a result of premature PCD in the tapetum and consequently in the sporogenic cells. Autophagy, via macroautophagy, occurs in the sporogenic cells and involves the formation of autophagosomes, through rough endoplasmic reticulum, and of complex macroautophagic structures. In the final stage of PCD, massive autophagy takes place. Male sterility in female individuals is thus reasonably interpreted as sporophytic CMS associated to autophagy.
Additional keywords: autophagy, cytochemistry, flower, PCD, sterility, TUNEL, ultrastructure, vacuolar cell death.
References
Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. The Plant Cell 13, 1803–1818.| The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsFKiu78%3D&md5=774d7567222486972a5202de37248d5fCAS |
Benevides CR, Haddad IVN, Barreira NP, Rodarte ATA, Galetto L, Santiag-Fernandes LDR, Lima HA (2013) Maytenus obtusifolia Mart. (Celastraceae): a tropical woody species in a transitional evolutionary stage of the gynodioecy–dioecy pathway. Plant Systematics and Evolution 299, 1693–1707.
| Maytenus obtusifolia Mart. (Celastraceae): a tropical woody species in a transitional evolutionary stage of the gynodioecy–dioecy pathway.Crossref | GoogleScholarGoogle Scholar |
Bergman P, Edqvist J, Farbos I, Glimelius K (2000) Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Molecular Biology 42, 531–544.
| Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivFKmtbc%3D&md5=a2cd08ebd1e10a719f0cae902baab6e6CAS |
Bino RJ (1985) Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida. Protoplasma 127, 230–240.
| Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida.Crossref | GoogleScholarGoogle Scholar |
Cortez PA, Carmello-Guerreiro SM, Teixeira SP (2012) Understanding male sterility in Miconia species (Melastomataceae): a morphological approach. Australian Journal of Botany 60, 506–516.
| Understanding male sterility in Miconia species (Melastomataceae): a morphological approach.Crossref | GoogleScholarGoogle Scholar |
Evert RF (2006) ‘Esau’s plant anatomy, meristems, cells, and tissues of the plant body: their structure, function, and development.’ (John Wiley & Sons Inc.: Hoboken, NJ, USA)
Falasca G, Angeli SD, Biasi R, Fattorini L, Matteucci M, Canini A, Altamura MM (2013) Tapetum and middle layer control male fertility in Actinidia deliciosa. Annals of Botany 112, 1045–1055.
| Tapetum and middle layer control male fertility in Actinidia deliciosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFyns7rK&md5=8fe9521a4c0073dc4537a37f2ff671f2CAS |
Flores-Rentería L, Orozco-Arroyo G, Cruz-García F, García-Campusano F, Alfaro I, Vázquez-Santana S (2013) Programmed cell death promotes male sterility in the functional dioecious Opuntia stenopetala (Cactaceae). Annals of Botany 112, 789–800.
| Programmed cell death promotes male sterility in the functional dioecious Opuntia stenopetala (Cactaceae).Crossref | GoogleScholarGoogle Scholar |
Gabe M (1968) ‘Techiniques histologiques.’ (Masson & Cie: Paris)
Gahan PB (1984) ‘Plant histochemistry and cytochemistry: an introduction.’ (Academic Press Inc.: London)
Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in-situ via specific labeling of nuclear DNA fragmentation. Journal of Cell Biology 119, 493–501.
| Identification of programmed cell death in-situ via specific labeling of nuclear DNA fragmentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtVyhsbs%3D&md5=ea610fae5f0b5dfa86b2e253600a47a6CAS |
González-Melendi P, Uyttewaal M, Morcillo CN, Mora JRH, Fajardo S, Budar F, Lucas MM (2008) A light and electron microscopy analysis of the events leading to male sterility in Ogu-INRA CMS of rape seed (Brassica napus). Journal of Experimental Botany 59, 827–838.
| A light and electron microscopy analysis of the events leading to male sterility in Ogu-INRA CMS of rape seed (Brassica napus).Crossref | GoogleScholarGoogle Scholar |
Hanamata S, Kurusu T, Kuchitsu K (2014) Roles of autophagy in male reproductive development in plants. Frontiers in Plant Science 5, 1–6.
| Roles of autophagy in male reproductive development in plants.Crossref | GoogleScholarGoogle Scholar |
Hernould M, Suharsono S, Zabaleta E, Carde JP, Litvak S, Araya A, Mouras A (1998) Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Molecular Biology 36, 499–508.
| Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1eltL8%3D&md5=a77dfe74f364bc96e60601e827949fe6CAS |
Hu J, Huang W, Huang Q, Qin X, Yu C, Wang L, Li S, Zhu R, Zhu Y (2014) Mitochondria and cytoplasmic male sterility in plants. Mitochondrion 19, 282–288.
| Mitochondria and cytoplasmic male sterility in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkslGhtb4%3D&md5=9017553693986a992930c75b80fd53b3CAS |
Jones AM, Dangl JL (1996) Logjam at the Styx: programmed cell death in plants. Trends in Plant Science 1, 114–119.
| Logjam at the Styx: programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar |
Karnovsky M (1965) A formaldehyde-gluraldehyde fixative of high osmolality for use in electron microscopy. Abstracts of Papers Presented at the Fifth Annual Meeting: The American Society for Cell Biology. Journal of Cell Biology 27, 137–138.
Kawanabe T, Ariizumi T, Kawai-Yamada M, Uchimiya H, Toriyama K (2006) Abolition of the tapetum suicide program ruins microsporogenesis. Plant & Cell Physiology 47, 784–787.
| Abolition of the tapetum suicide program ruins microsporogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVCgsro%3D&md5=c6f28dd77a968f9a8127235c59e5299eCAS |
Ku S, Yoon H, Suh HS, Chung Y-Y (2003) Male-sterility of thermo sensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217, 559–565.
| Male-sterility of thermo sensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVWgsLg%3D&md5=9fcecbbc8957e472cfde86788495efc8CAS |
Latrasse D, Benhamed M, Bergounioux C, Raynaud C, Delarue M (2016) Plant programmed cell death from a chromatin point of view. Journal of Experimental Botany 67, 5887–5900.
| Plant programmed cell death from a chromatin point of view.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhsVygtbg%3D&md5=75c030588a2210a1583414737dfe64e4CAS |
Li N, Zhang D-S, Liu H-S, Yin C-S, Li X-x, Liang W-q, Yuan Z, Xu B, Chu H-W, Wang J, Wen T-Q, Huang H, Luo D, Ma H, Zhang D-B (2006) The Rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. The Plant Cell 18, 2999–3014.
| The Rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1CltQ%3D%3D&md5=1fce5ff0f005c540eb1c4d083cfa55dfCAS |
Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology 63, 215–237.
| Autophagy: pathways for self-eating in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1ams7g%3D&md5=1eac94a411275dccf5f259607ac0958cCAS |
Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. International Journal of Biochemistry & Cell Biology 36, 2405–2419.
| Apoptosis, autophagy, and more.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFemu78%3D&md5=67717f916b559ee38c31309033d4197eCAS |
Luo XD, Dai LF, Wang SB, Wolukau JN, Jahn M, Chen JF (2006) Male gamete development and early tapetal degeneration in cytoplasmic male-sterile pepper investigated by meiotic, anatomical and ultrastructural analyses. Plant Breeding 125, 395–399.
| Male gamete development and early tapetal degeneration in cytoplasmic male-sterile pepper investigated by meiotic, anatomical and ultrastructural analyses.Crossref | GoogleScholarGoogle Scholar |
Majewska-Sawka A, Rodriguez-Garcia MI, Nakashima H, Jassen B (1993) Ultrastructural expression of cytoplasmic male sterility in sugar beet (Beta vulgaris L.). Sexual Plant Reproduction 6, 22–32.
| Ultrastructural expression of cytoplasmic male sterility in sugar beet (Beta vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Papini A, Mosti S, Brighigna L (1999) Programmed cell death events during tapetum development of angiosperms. Protoplasma 207, 213–221.
| Programmed cell death events during tapetum development of angiosperms.Crossref | GoogleScholarGoogle Scholar |
Peled-Zehavi H, Galili G (2018) Fluorescence imaging of autophagy-mediated ER-to-vacuole trafficking in plants. In ‘The plant endoplasmic reticulum. Vol. 1691’. (Eds C Hawes, V Kriechbaumer) pp. 239–249 (Humana Press: New York)
Polowick PL, Sawhney VK (1990) Microsporogenesis in a normal line and in the ogu cytoplasmic male-sterile line of Brassica napus. Sexual Plant Reproduction 3, 263–276.
| Microsporogenesis in a normal line and in the ogu cytoplasmic male-sterile line of Brassica napus.Crossref | GoogleScholarGoogle Scholar |
Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. Journal of Experimental Botany 59, 435–444.
| Programmed cell death in plants: distinguishing between different modes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVamu7g%3D&md5=7144289cd6f8fbdae101358be3eb7ba4CAS |
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208–212.
| The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXktVClu70%3D&md5=8f4845c8d2664c4b77379632b7a7c5f0CAS |
Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of F1FO-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Reports 4, 381–386.
| ORFB is a subunit of F1FO-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFajs74%3D&md5=8cfee3be461f21c4b4ca3a12a3588e90CAS |
Schulz PJ, Cross JW, Almeida E (1993) Chemical agents that inhibit pollen development: effects of the phenylcinnoline carboxylates SC-1058 and SC-1271 on the ultrastructure of developing wheat anthers (Triticum aestivum L. var Yecorarojò). Sexual Plant Reproduction 6, 108–212.
| Chemical agents that inhibit pollen development: effects of the phenylcinnoline carboxylates SC-1058 and SC-1271 on the ultrastructure of developing wheat anthers (Triticum aestivum L. var Yecorarojò).Crossref | GoogleScholarGoogle Scholar |
Shi Y, Zhao S, Yao J (2009) Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice. Journal of Integrative Plant Biology 51, 774–781.
| Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice.Crossref | GoogleScholarGoogle Scholar |
Shi S, Ding D, Mei S, Wang J (2010) A comparative light and electron microscopic analysis of microspore and tapetum development in fertile and cytoplasmic male sterile radish. Protoplasma 241, 37–49.
| A comparative light and electron microscopic analysis of microspore and tapetum development in fertile and cytoplasmic male sterile radish.Crossref | GoogleScholarGoogle Scholar |
Smith AR, Zhao D (2016) Sterility caused by floral organ degeneration and abiotic stresses in Arabidopsis and cereal grains. Frontiers in Plant Science 7, 1503
| Sterility caused by floral organ degeneration and abiotic stresses in Arabidopsis and cereal grains.Crossref | GoogleScholarGoogle Scholar |
Strittmatter LI, Negrón-Ortiz V, Hickey JR (2006) Comparative microsporangium development in male-fertile and male-sterile flowers of Consolea (Cactaceae): when and how does pollen abortion occur. Grana 45, 81–100.
| Comparative microsporangium development in male-fertile and male-sterile flowers of Consolea (Cactaceae): when and how does pollen abortion occur.Crossref | GoogleScholarGoogle Scholar |
Toyooka K, Matsuoka K (2006) Autophagy and non-classical vacuolar targeting in tobacco BY-2 cells. In ‘Tobacco BY-2 cells: from cellular dynamics to omics. Biotechnology in Agriculture and Forestry. Vol. 58’. (Eds T Nagata, K Matsuoka, D Inzé) pp. 167–180. (Springer: Berlin)
Üstün S, Hafrén A, Hofius D (2017) Autophagy as a mediator of life and death in plants. Current Opinion in Plant Biology 40, 122–130.
| Autophagy as a mediator of life and death in plants.Crossref | GoogleScholarGoogle Scholar |
van Doorn WG, Papini A (2013) Ultrastructure of autophagy in plant cells. Autophagy 9, 1922–1936.
| Ultrastructure of autophagy in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyrtbfN&md5=f50adf80cafb9349e3d00a24c71407a5CAS |
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, 1241–1246.
| Morphological classification of plant cell deaths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1Gku7w%3D&md5=1369af328f1ea4d2cd1c6e7885d92ab2CAS |
Wu H-m, Cheung AY (2000) Programmed cell death in plant reproduction. Plant Molecular Biology 44, 267–281.
| Programmed cell death in plant reproduction.Crossref | GoogleScholarGoogle Scholar |
Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant & Cell Physiology 53, 1355–1365.
| Beginning to understand autophagy, an intracellular self-degradation system in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1egurrF&md5=5a3a1adc6ca97fb46b2420f356ae9e9eCAS |
