← Back to Search
Boosting Autophagy In Sexual Reproduction: A Plant Perspective.
Shanshan Li, He Yan, Wei-Ming Mei, Y. C. Tse, H. Wang
Published 2020 · Biology, Medicine
Download PDFAnalyze on Scholarcy
The key process of sexual reproduction is the successful fusion of the sperm and egg cell. Distinct from dynamic and flagellated animal sperm cells, higher flowering plant sperm cells are immotile. Therefore, plants have evolved a novel reproductive system to achieve fertilization and generate progenies. Plant sexual reproduction consists of multiple steps mainly including gametophyte development, pollen-pistil recognition, pollen germination, double fertilization and post-fertilization. During reproduction, active production, consumption and recycling of cellular components and energy are critically required to achieve fertilization. However, the underlying machinery of cellular degradation and turnover remains largely unexplored. Autophagy, the major catabolic pathway in eukaryotic cells, participates in regulating multiple aspects of plant activities including abiotic and biotic stress resistance, pathogen response, senescence, nutrient remobilization and plant development. Nevertheless, a key unanswered question is how autophagy regulates plant fertilization and reproduction. Here, we focus on comparing and contrasting autophagy in several key reproductive processes of plant and animal systems to feature important distinctions and highlight future research directions of autophagy in angiosperm reproduction. We further discuss the potential crosstalk between autophagy and programmed cell death that are often considered as two disconnected events in plant sexual reproduction.
This paper references
Comparative analyses of ubiquitin-like ATG8 and cysteine protease ATG4 autophagy genes in the plant lineage and cross-kingdom processing of ATG8 by ATG4
Eunyoung Seo (2016)
Vacuolar Trafficking Protein VPS38 Is Dispensable for Autophagy1[OPEN]
Han Nim Lee (2017)
A brief history of autophagy from cell biology to physiology and disease
N. Mizushima (2018)
Arabidopsis ATG6 is required to limit the pathogen-associated cell death response
S. Patel (2008)
Defective autophagy through epg5 mutation results in failure to reduce germ plasm and mitochondria
A. Herpin (2015)
Proteomic analysis of steroid-triggered autophagic programmed cell death during Drosophila development
D. Martin (2007)
The Vacuolar Protein Sorting-38 Subunit of the Arabidopsis Phosphatidylinositol-3-Kinase Complex Plays Critical Roles in Autophagy, Endosome Sorting, and Gravitropism
F. Liu (2018)
Autophagy mitigates high-temperature injury in pollen development of Arabidopsis thaliana.
Gonul Dundar (2019)
Cytoplasmic connection of sperm cells to the pollen vegetative cell nucleus: potential roles of the male germ unit revisited.
Andrea D McCue (2011)
The ubiquitin 26S proteasome proteolytic pathway.
J. Smalle (2004)
NaStEP: A Proteinase Inhibitor Essential to Self-Incompatibility and a Positive Regulator of HT-B Stability in Nicotiana alata Pollen Tubes1[W][OA]
K. Jiménez-Durán (2012)
Atg8, a Ubiquitin-like Protein Required for Autophagosome Formation, Mediates Membrane Tethering and Hemifusion
H. Nakatogawa (2007)
Expression of Autophagy-associated ATG8 Genes during Petal Senescence in Japanese Morning Glory
K. Shibuya (2011)
Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species.
Alejandro Tovar-Méndez (2014)
Functions and Regulation of Programmed Cell Death in Plant Development.
Anna Daneva (2016)
Heatmapper: web-enabled heat mapping for all
Sasha Babicki (2016)
An Arabidopsis Homolog of Yeast ATG6/VPS30 Is Essential for Pollen Germination1[W]
Y. Fujiki (2007)
The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants.
S. Sláviková (2005)
Another way to die: autophagic programmed cell death
Y. Tsujimoto (2005)
Live to die another way: modes of programmed cell death and the signals emanating from dying cells
Yaron Fuchs (2015)
Prohibitin 2 Is an Inner Mitochondrial Membrane Mitophagy Receptor
Yongjie Wei (2017)
Autophagy regulates spermatid differentiation via degradation of PDLIM1
Y. Shang (2016)
Autophagy in sexual plant reproduction as an emerging field
P. Zhao (2016)
Autophagy and metacaspase determine the mode of cell death in plants
E. Minina (2013)
Pollen vacuoles and their significance
E. Pacini (2011)
Autophagy is required for necrotic cell death in Caenorhabditis elegans
C. Samara (2008)
Plant Bax Inhibitor-1 interacts with ATG6 to regulate autophagy and programmed cell death
Guoyong Xu (2017)
Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes
Huiwu Tang (2017)
ATG8 Expansion: A Driver of Selective Autophagy Diversification?
Ronny Kellner (2017)
The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits in Arabidopsis[C][W]
E. Indriolo (2014)
Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans
Q. Zhou (2011)
Specification of tapetum and microsporocyte cells within the anther.
D. Zhang (2014)
Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana
N. Harrison-Lowe (2008)
Mitochondrial dynamics in plant male gametophyte visualized by fluorescent live imaging.
R. Matsushima (2008)
Assortment of phosphatidylinositol 3-kinase complexes--Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae.
K. Obara (2006)
Morphological changes in senescing petal cells and the regulatory mechanism of petal senescence.
Kenichi Shibuya (2016)
Autophagy Is Essential for Preimplantation Development of Mouse Embryos
S. Tsukamoto (2008)
Autophagy: The Master of Bulk and Selective Recycling.
R. S. Marshall (2018)
The suspensor as a model system to study the mechanism of cell fate specification during early embryogenesis
X. Peng (2018)
OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development
T. Kurusu (2014)
Herkogamy and Its Effects on Mating Patterns in Arabidopsis thaliana
Yonghai Luo (2013)
Elevation of Pollen Mitochondrial DNA Copy Number by WHIRLY2: Altered Respiration and Pollen Tube Growth in Arabidopsis1
Q. Cai (2015)
Pollination induces autophagy in petunia petals via ethylene
K. Shibuya (2013)
Paternal mitochondrial destruction after fertilization is mediated by a common endocytic and autophagic pathway in Drosophila.
Yoav Politi (2014)
The ARC1 E3 Ligase Gene Is Frequently Deleted in Self-Compatible Brassicaceae Species and Has a Conserved Role in Arabidopsis lyrata Self-Pollen Rejection[W]
E. Indriolo (2012)
Autophagy controls resource allocation and protein storage accumulation in Arabidopsis seeds
Julien Di Berardino (2018)
InPSR26, a Putative Membrane Protein, Regulates Programmed Cell Death during Petal Senescence in Japanese Morning Glory1[W][OA]
Kenichi Shibuya (2008)
Taking one for the team: self-recognition and cell suicide in pollen.
Katie A Wilkins (2014)
Modulation of plant autophagy during pathogen attack.
Alexandre Y Leary (2018)
Exocyst, exosomes, and autophagy in the regulation of Brassicaceae pollen-stigma interactions.
D. Goring (2017)
Atg7 is required for acrosome biogenesis during spermatogenesis in mice
H. Wang (2014)
A BAR-Domain Protein SH3P2, Which Binds to Phosphatidylinositol 3-Phosphate and ATG8, Regulates Autophagosome Formation in Arabidopsis[C][W]
Xiaohong Zhuang (2013)
Autophagy as initiator or executioner of cell death.
E. Minina (2014)
Evidence for contribution of autophagy to rubisco degradation during leaf senescence in Arabidopsis thaliana.
Y. Ono (2013)
Developmental role of the tomato Mediator complex subunit MED18 in pollen ontogeny.
F. Pérez-Martín (2018)
A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development.
Chonghui Ji (2013)
N-terminal β-strand underpins biochemical specialization of an ATG8 isoform
Erin K Zess (2019)
Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics.
Yan Zhang (2011)
DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis
A. Plackett (2014)
Spatial and temporal transcriptome changes occurring during flower opening and senescence of the ephemeral hibiscus flower, Hibiscus rosa-sinensis
Alice Trivellini (2016)
Postfertilization Autophagy of Sperm Organelles Prevents Paternal Mitochondrial DNA Transmission
Sara Al Rawi (2011)
Fertilization Mechanisms in Flowering Plants
T. Dresselhaus (2016)
Autophagy-mediated regulation of phytohormone metabolism during rice anther development
T. Kurusu (2017)
Vacuolar sorting receptors (VSRs) and secretory carrier membrane proteins (SCAMPs) are essential for pollen tube growth.
H. Wang (2010)
A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues
Xue-mei Zhou (2015)
Atg8 family LC3/GABARAP proteins are crucial for autophagosome–lysosome fusion but not autophagosome formation during PINK1/Parkin mitophagy and starvation
T. N. Nguyen (2016)
Self-incompatibility in plants.
S. Takayama (2005)
Differential processing of Arabidopsis ubiquitin-like Atg8 autophagy proteins by Atg4 cysteine proteases
Jongchan Woo (2013)
Autophagy is activated and involved in cell death with participation of cathepsins during stress-induced microspore embryogenesis in barley
I. Bárány (2018)
Mitochondrial endonuclease G mediates breakdown of paternal mitochondria upon fertilization
Q. Zhou (2016)
Self-consumption: the interplay of autophagy and apoptosis
G. Marin͂o (2014)
Identification of transcription factors that regulate ATG8 expression and autophagy in Arabidopsis
P. Wang (2019)
Abolition of the tapetum suicide program ruins microsporogenesis.
T. Kawanabe (2006)
Modulation of autophagy and protease activities by small bioactive compounds to reduce cell death and improve stress-induced microspore embryogenesis initiation in rapeseed and barley
Y. Pérez-Pérez (2019)
Persistence and Protection of Mitochondrial DNA in the Generative Cell of Cucumber is Consistent with its Paternal Transmission.
J. Shen (2015)
Secretory Activity Is Rapidly Induced in Stigmatic Papillae by Compatible Pollen, but Inhibited for Self-Incompatible Pollen in the Brassicaceae
D. Safavian (2013)
Autophagy is required for gamete differentiation in the moss Physcomitrella patens
Victoria Sanchez-Vera (2017)
A unique program for cell death in xylem fibers of Populus stem.
C. Courtois-Moreau (2009)
Autophagy Is Enhanced and Floral Development Is Impaired in AtHVA22d RNA Interference Arabidopsis[C][W][OA]
C. Chen (2009)
Roles of autophagy in male reproductive development in plants
Shigeru Hanamata (2014)
Somatic embryogenesis: life and death processes during apical-basal patterning.
A. Smertenko (2014)
Autophagy: a multifaceted intracellular system for bulk and selective recycling.
Faqiang Li (2012)
Stamen Structure and Function
R. Scott (2004)
Petal micromorphology and its relationship to pollination.
V. Costa (2017)
Germ cell-specific Atg7 knockout results in primary ovarian insufficiency in female mice
Z. Song (2015)
Lysosome: The metabolic signaling hub
D. Lamming (2019)
Germline specification and function in plants.
F. Berger (2011)
Corrigendum: Autophagy-related approaches for improving nutrient use efficiency and crop yield protection.
Tamar Avin-Wittenberg (2018)
An Autophagy-Related Kinase Is Essential for the Symbiotic Relationship between Phaseolus vulgaris and Both Rhizobia and Arbuscular Mycorrhizal Fungi[OPEN]
Georgina Estrada-Navarrete (2016)
Plant autophagy: new flavors on the menu.
X. Ding (2018)
Pollen Acceptance or Rejection: A Tale of Two Pathways.
Jennifer Doucet (2016)
Autophagy in C. elegans development.
N. J. Palmisano (2019)
Cell mechanics of pollen tube growth.
Christine L. Cameron (2018)
Arabidopsis AtVPS15 plays essential roles in pollen germination possibly by interacting with AtVPS34.
Wei-ying Wang (2012)
Clearance of Parental Products.
P. Svoboda (2017)
Linking Autophagy to Abiotic and Biotic Stress Responses.
S. Signorelli (2019)
Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots.
L. R. D. Craene (2007)
Transcriptome analysis of embryonic domains in Norway spruce reveals potential regulators of suspensor cell death
Salim H Reza (2018)
Arabidopsis AtBECLIN 1/AtAtg6/AtVps30 is essential for pollen germination and plant development
Genji Qin (2007)
Male sterility and fertility restoration in crops.
L. Chen (2014)
Licarin A induces cell death by activation of autophagy and apoptosis in non-small cell lung cancer cells
U. Maheswari (2018)
Vacuolar cell death in plants
E. Minina (2014)
Regulation of ATG6/Beclin-1 homologs by abiotic stresses and hormones in rice (Oryza sativa L.).
R. Rana (2012)