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Article: MS1/MMD1 homologues in the moss Physcomitrium patens are required for male and female gametogenesis

Landberg, Katarina / Lopez‐Obando, Mauricio / Sanchez Vera, Victoria / Sundberg, Eva / Thelander, Mattias

The new phytologist. 2022 Oct., v. 236, no. 2

2022

Abstract: The Arabidopsis Plant HomeoDomain (PHD) proteins AtMS1 and AtMMD1 provide chromatin‐mediated transcriptional regulation essential for tapetum‐dependent pollen formation. This pollen‐based male gametogenesis is a derived trait of seed plants. Male ... ...

Abstract	The Arabidopsis Plant HomeoDomain (PHD) proteins AtMS1 and AtMMD1 provide chromatin‐mediated transcriptional regulation essential for tapetum‐dependent pollen formation. This pollen‐based male gametogenesis is a derived trait of seed plants. Male gametogenesis in the common ancestors of land plants is instead likely to have been reminiscent of that in extant bryophytes where flagellated sperms are produced by an elaborate gametophyte generation. Still, also bryophytes possess MS1/MMD1‐related PHD proteins. We addressed the function of two MS1/MMD1‐homologues in the bryophyte model moss Physcomitrium patens by the generation and analysis of reporter and loss‐of‐function lines. The two genes are together essential for both male and female fertility by providing functions in the gamete‐producing inner cells of antheridia and archegonia. They are furthermore expressed in the diploid sporophyte generation suggesting a function during sporogenesis, a process proposed related by descent to pollen formation in angiosperms. We propose that the moss MS1/MMD1‐related regulatory network required for completion of male and female gametogenesis, and possibly for sporogenesis, represent a heritage from ancestral land plants.
Keywords	Arabidopsis ; Physcomitrium ; diploidy ; female fertility ; females ; gametogenesis ; gametophytes ; loss-of-function mutation ; males ; mosses and liverworts ; pollen ; sporophytes ; sporulation ; transcription (genetics)
Language	English
Dates of publication	2022-10
Size	p. 512-524.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18352
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: MS1/MMD1 homologues in the moss Physcomitrium patens are required for male and female gametogenesis.

Landberg, Katarina / Lopez-Obando, Mauricio / Sanchez Vera, Victoria / Sundberg, Eva / Thelander, Mattias

The New phytologist

2022 Volume 236, Issue 2, Page(s) 512–524

Abstract: The Arabidopsis Plant HomeoDomain (PHD) proteins AtMS1 and AtMMD1 provide chromatin-mediated transcriptional regulation essential for tapetum-dependent pollen formation. This pollen-based male gametogenesis is a derived trait of seed plants. Male ... ...

Abstract	The Arabidopsis Plant HomeoDomain (PHD) proteins AtMS1 and AtMMD1 provide chromatin-mediated transcriptional regulation essential for tapetum-dependent pollen formation. This pollen-based male gametogenesis is a derived trait of seed plants. Male gametogenesis in the common ancestors of land plants is instead likely to have been reminiscent of that in extant bryophytes where flagellated sperms are produced by an elaborate gametophyte generation. Still, also bryophytes possess MS1/MMD1-related PHD proteins. We addressed the function of two MS1/MMD1-homologues in the bryophyte model moss Physcomitrium patens by the generation and analysis of reporter and loss-of-function lines. The two genes are together essential for both male and female fertility by providing functions in the gamete-producing inner cells of antheridia and archegonia. They are furthermore expressed in the diploid sporophyte generation suggesting a function during sporogenesis, a process proposed related by descent to pollen formation in angiosperms. We propose that the moss MS1/MMD1-related regulatory network required for completion of male and female gametogenesis, and possibly for sporogenesis, represent a heritage from ancestral land plants.
MeSH term(s)	Arabidopsis/genetics ; Bryopsida/genetics ; Bryopsida/metabolism ; Chromatin/metabolism ; Distal Myopathies ; Gametogenesis ; Gene Expression Regulation, Plant ; Muscular Atrophy ; Plants/genetics
Chemical Substances	Chromatin
Language	English
Publishing date	2022-07-16
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18352
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Autophagy Is Required for Strawberry Fruit Ripening.

Sánchez-Sevilla, José F / Botella, Miguel A / Valpuesta, Victoriano / Sanchez-Vera, Victoria

Frontiers in plant science

2021 Volume 12, Page(s) 688481

Abstract: Autophagy is a catabolic and recycling pathway that maintains cellular homeostasis under normal growth and stress conditions. Two major types of autophagy, microautophagy and macroautophagy, have been described in plants. During macroautophagy, cellular ... ...

Abstract	Autophagy is a catabolic and recycling pathway that maintains cellular homeostasis under normal growth and stress conditions. Two major types of autophagy, microautophagy and macroautophagy, have been described in plants. During macroautophagy, cellular content is engulfed by a double-membrane vesicle called autophagosome. This vesicle fuses its outer membrane with the tonoplast and releases the content into the vacuole for degradation. During certain developmental processes, autophagy is enhanced by induction of several autophagy-related genes (
Language	English
Publishing date	2021-08-27
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2021.688481
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

Sanchez‐Vera, Victoria / Landberg, Katarina / Lopez‐Obando, Mauricio / Thelander, Mattias / Lagercrantz, Ulf / Muñoz‐Viana, Rafael / Schmidt, Anja / Grossniklaus, Ueli / Sundberg, Eva

The new phytologist. 2022 Mar., v. 233, no. 6

2022

Abstract: Although land plant germ cells have received much attention, knowledge about their specification is still limited. We thus identified transcripts enriched in egg cells of the bryophyte model species Physcomitrium patens, compared the results with ... ...

Abstract	Although land plant germ cells have received much attention, knowledge about their specification is still limited. We thus identified transcripts enriched in egg cells of the bryophyte model species Physcomitrium patens, compared the results with angiosperm egg cells, and selected important candidate genes for functional analysis. We used laser‐assisted microdissection to perform a cell‐type‐specific transcriptome analysis on egg cells for comparison with available expression profiles of vegetative tissues and male reproductive organs. We made reporter lines and knockout mutants of the two BONOBO (PbBNB) genes and studied their role in reproduction. We observed an overlap in gene activity between bryophyte and angiosperm egg cells, but also clear differences. Strikingly, several processes that are male‐germline specific in Arabidopsis are active in the P. patens egg cell. Among those were the moss PbBNB genes, which control proliferation and identity of both female and male germlines. Pathways shared between male and female germlines were most likely present in the common ancestors of land plants, besides sex‐specifying factors. A set of genes may also be involved in the switches between the diploid and haploid moss generations. Nonangiosperm gene networks also contribute to the specification of the P. patens egg cell.
Keywords	Arabidopsis ; Physcomitrium ; cell specificity ; diploidy ; eggs ; epigenetics ; females ; genes ; haploidy ; males ; microdissection ; mosses and liverworts ; ova ; reproduction ; transcriptomics
Language	English
Dates of publication	2022-03
Size	p. 2614-2628.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.17938
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification.

Sanchez-Vera, Victoria / Landberg, Katarina / Lopez-Obando, Mauricio / Thelander, Mattias / Lagercrantz, Ulf / Muñoz-Viana, Rafael / Schmidt, Anja / Grossniklaus, Ueli / Sundberg, Eva

The New phytologist

2022 Volume 233, Issue 6, Page(s) 2614–2628

Abstract	Although land plant germ cells have received much attention, knowledge about their specification is still limited. We thus identified transcripts enriched in egg cells of the bryophyte model species Physcomitrium patens, compared the results with angiosperm egg cells, and selected important candidate genes for functional analysis. We used laser-assisted microdissection to perform a cell-type-specific transcriptome analysis on egg cells for comparison with available expression profiles of vegetative tissues and male reproductive organs. We made reporter lines and knockout mutants of the two BONOBO (PbBNB) genes and studied their role in reproduction. We observed an overlap in gene activity between bryophyte and angiosperm egg cells, but also clear differences. Strikingly, several processes that are male-germline specific in Arabidopsis are active in the P. patens egg cell. Among those were the moss PbBNB genes, which control proliferation and identity of both female and male germlines. Pathways shared between male and female germlines were most likely present in the common ancestors of land plants, besides sex-specifying factors. A set of genes may also be involved in the switches between the diploid and haploid moss generations. Nonangiosperm gene networks also contribute to the specification of the P. patens egg cell.
MeSH term(s)	Bryopsida/genetics ; Bryopsida/metabolism ; Epigenesis, Genetic ; Germ Cells, Plant
Language	English
Publishing date	2022-01-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.17938
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Autophagy is required for gamete differentiation in the moss Physcomitrella patens.

Sanchez-Vera, Victoria / Kenchappa, Chandra Shekar / Landberg, Katarina / Bressendorff, Simon / Schwarzbach, Stefan / Martin, Tom / Mundy, John / Petersen, Morten / Thelander, Mattias / Sundberg, Eva

Autophagy

2017 Volume 13, Issue 11, Page(s) 1939–1951

Abstract: Autophagy, a major catabolic process in eukaryotes, was initially related to cell tolerance to nutrient depletion. In plants autophagy has also been widely related to tolerance to biotic and abiotic stresses (through the induction or repression of ... ...

Abstract	Autophagy, a major catabolic process in eukaryotes, was initially related to cell tolerance to nutrient depletion. In plants autophagy has also been widely related to tolerance to biotic and abiotic stresses (through the induction or repression of programmed cell death, PCD) as well as to promotion of developmentally regulated PCD, starch degradation or caloric restriction important for life span. Much less is known regarding its role in plant cell differentiation. Here we show that macroautophagy, the autophagy pathway driven by engulfment of cytoplasmic components by autophagosomes and its subsequent degradation in vacuoles, is highly active during germ cell differentiation in the early diverging land plant Physcomitrella patens. Our data provide evidence that suppression of ATG5-mediated autophagy results in reduced density of the egg cell-mediated mucilage that surrounds the mature egg, pointing toward a potential role of autophagy in extracellular mucilage formation. In addition, we found that ATG5- and ATG7-mediated autophagy is essential for the differentiation and cytoplasmic reduction of the flagellated motile sperm and hence for sperm fertility. The similarities between the need of macroautophagy for sperm differentiation in moss and mouse are striking, strongly pointing toward an ancestral function of autophagy not only as a protector against nutrient stress, but also in gamete differentiation.
MeSH term(s)	Autophagy/genetics ; Autophagy-Related Protein 5/metabolism ; Autophagy-Related Protein 7/metabolism ; Bryopsida/cytology ; Bryopsida/genetics ; Cell Differentiation ; Gene Expression Regulation, Plant ; Germ Cells, Plant/cytology ; Plant Mucilage/metabolism ; Stress, Physiological
Chemical Substances	Autophagy-Related Protein 5 ; Plant Mucilage ; Autophagy-Related Protein 7 (EC 6.2.1.45)
Language	English
Publishing date	2017-09-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2454135-7
ISSN	1554-8635 ; 1554-8627
ISSN (online)	1554-8635
ISSN	1554-8627
DOI	10.1080/15548627.2017.1366406
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Detection and measurement of necrosis in plants.

Minina, Elena A / Filonova, Lada H / Sanchez-Vera, Victoria / Suarez, Maria F / Daniel, Geoffrey / Bozhkov, Peter V

Methods in molecular biology (Clifton, N.J.)

2013 Volume 1004, Page(s) 229–248

Abstract: Necrosis plays a fundamental role in plant physiology and pathology. When plants or plant cell cultures are subjected to abiotic stress they initiate rapid cell death with necrotic morphology. Likewise, when plants are attacked by pathogens, they develop ...

Abstract	Necrosis plays a fundamental role in plant physiology and pathology. When plants or plant cell cultures are subjected to abiotic stress they initiate rapid cell death with necrotic morphology. Likewise, when plants are attacked by pathogens, they develop necrotic lesions, the reaction known as hypersensitive response. Great advances in the understanding of signaling pathways that lead to necrosis during plant-pathogen interaction have been made in the last two decades using Arabidopsis thaliana as a model plant. Further understanding of these signaling pathways, as well as those regulating the execution phase of necrotic cell death per se would require a robust set of readout assays to detect and measure necrosis in various plant model systems. Here we provide description of such assays, beginning from electron microscopy, as the "gold standard" to diagnose necrosis. This is followed by two groups of biochemical and cytochemical assays used by our group to detect and quantify mitochondrial dysfunction and the loss of protoplast integrity during necrosis in Arabidopsis plants and cell suspension cultures of both Arabidopsis and Norway spruce.
MeSH term(s)	Adenosine Triphosphate/metabolism ; Arabidopsis/cytology ; Arabidopsis/ultrastructure ; Cell Survival ; Cells, Cultured ; Cytological Techniques/methods ; Fluorescent Dyes/metabolism ; Intracellular Space/metabolism ; Ions ; Mitochondria/metabolism ; Mitochondria/ultrastructure ; Necrosis ; Oxygen Consumption ; Picea/cytology ; Picea/embryology ; Picea/ultrastructure ; Protoplasts/metabolism ; Reactive Oxygen Species/metabolism ; Suspensions
Chemical Substances	Fluorescent Dyes ; Ions ; Reactive Oxygen Species ; Suspensions ; Adenosine Triphosphate (8L70Q75FXE)
Language	English
Publishing date	2013
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-62703-383-1_17
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Autophagy mediates caloric restriction-induced lifespan extension in Arabidopsis.

Minina, Elena A / Sanchez-Vera, Victoria / Moschou, Panagiotis N / Suarez, Maria F / Sundberg, Eva / Weih, Martin / Bozhkov, Peter V

Aging cell

2013 Volume 12, Issue 2, Page(s) 327–329

Abstract: Caloric restriction (CR) extends lifespan in various heterotrophic organisms ranging from yeasts to mammals, but whether a similar phenomenon occurs in plants remains unknown. Plants are autotrophs and use their photosynthetic machinery to convert light ... ...

Abstract	Caloric restriction (CR) extends lifespan in various heterotrophic organisms ranging from yeasts to mammals, but whether a similar phenomenon occurs in plants remains unknown. Plants are autotrophs and use their photosynthetic machinery to convert light energy into the chemical energy of glucose and other organic compounds. As the rate of photosynthesis is proportional to the level of photosynthetically active radiation, the CR in plants can be modeled by lowering light intensity. Here, we report that low light intensity extends the lifespan in Arabidopsis through the mechanisms triggering autophagy, the major catabolic process that recycles damaged and potentially harmful cellular material. Knockout of autophagy-related genes results in the short lifespan and suppression of the lifespan-extending effect of the CR. Our data demonstrate that the autophagy-dependent mechanism of CR-induced lifespan extension is conserved between autotrophs and heterotrophs.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/metabolism ; Arabidopsis/radiation effects ; Arabidopsis Proteins/genetics ; Autophagy/genetics ; Autophagy/radiation effects ; Autophagy-Related Protein 5 ; Caloric Restriction ; Glucose/metabolism ; Light ; Longevity/genetics ; Longevity/radiation effects ; Phosphoric Monoester Hydrolases/deficiency ; Phosphoric Monoester Hydrolases/genetics ; Photosynthesis/physiology ; Plants, Genetically Modified
Chemical Substances	Arabidopsis Proteins ; Autophagy-Related Protein 5 ; Atg5 protein, Arabidopsis (EC 3.1.3.-) ; Phosphoric Monoester Hydrolases (EC 3.1.3.2) ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2013-04
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2113083-8
ISSN	1474-9726 ; 1474-9718
ISSN (online)	1474-9726
ISSN	1474-9718
DOI	10.1111/acel.12048
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Article ; Online: EXTRA SPINDLE POLES (Separase) controls anisotropic cell expansion in Norway spruce (Picea abies) embryos independently of its role in anaphase progression.

Moschou, Panagiotis N / Savenkov, Eugene I / Minina, Elena A / Fukada, Kazutake / Reza, Salim Hossain / Gutierrez-Beltran, Emilio / Sanchez-Vera, Victoria / Suarez, Maria F / Hussey, Patrick J / Smertenko, Andrei P / Bozhkov, Peter V

The New phytologist

2016 Volume 212, Issue 1, Page(s) 232–243

Abstract: The caspase-related protease separase (EXTRA SPINDLE POLES, ESP) plays a major role in chromatid disjunction and cell expansion in Arabidopsis thaliana. Whether the expansion phenotypes are linked to defects in cell division in Arabidopsis ESP mutants ... ...

Abstract	The caspase-related protease separase (EXTRA SPINDLE POLES, ESP) plays a major role in chromatid disjunction and cell expansion in Arabidopsis thaliana. Whether the expansion phenotypes are linked to defects in cell division in Arabidopsis ESP mutants remains elusive. Here we present the identification, cloning and characterization of the gymnosperm Norway spruce (Picea abies, Pa) ESP. We used the P. abies somatic embryo system and a combination of reverse genetics and microscopy to explore the roles of Pa ESP during embryogenesis. Pa ESP was expressed in the proliferating embryonal mass, while it was absent in the suspensor cells. Pa ESP associated with kinetochore microtubules in metaphase and then with anaphase spindle midzone. During cytokinesis, it localized on the phragmoplast microtubules and on the cell plate. Pa ESP deficiency perturbed anisotropic expansion and reduced mitotic divisions in cotyledonary embryos. Furthermore, whilst Pa ESP can rescue the chromatid nondisjunction phenotype of Arabidopsis ESP mutants, it cannot rescue anisotropic cell expansion. Our data demonstrate that the roles of ESP in daughter chromatid separation and cell expansion are conserved between gymnosperms and angiosperms. However, the mechanisms of ESP-mediated regulation of cell expansion seem to be lineage-specific.
MeSH term(s)	Amino Acid Sequence ; Anaphase ; Anisotropy ; Cell Proliferation ; Chromosomes, Plant/genetics ; Cloning, Molecular ; Cytokinesis ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Gene Knockdown Techniques ; Microtubules/metabolism ; Phylogeny ; Picea/cytology ; Picea/embryology ; Picea/enzymology ; Plant Proteins/metabolism ; Protein Transport ; Seeds/cytology ; Seeds/embryology ; Seeds/enzymology ; Separase/metabolism ; Sequence Analysis, Protein
Chemical Substances	Plant Proteins ; Separase (EC 3.4.22.49)
Language	English
Publishing date	2016-05-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.14012
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness

Journal of experimental botany. 2018 Mar. 14, v. 69, no. 6

2018

Abstract: Autophagy is a major catabolic process whereby autophagosomes deliver cytoplasmic content to the lytic compartment for recycling. Autophagosome formation requires two ubiquitin-like systems conjugating Atg12 with Atg5, and Atg8 with lipid ... ...

Abstract	Autophagy is a major catabolic process whereby autophagosomes deliver cytoplasmic content to the lytic compartment for recycling. Autophagosome formation requires two ubiquitin-like systems conjugating Atg12 with Atg5, and Atg8 with lipid phosphatidylethanolamine (PE), respectively. Genetic suppression of these systems causes autophagy-deficient phenotypes with reduced fitness and longevity. We show that Atg5 and the E1-like enzyme, Atg7, are rate-limiting components of Atg8–PE conjugation in Arabidopsis. Overexpression of ATG5 or ATG7 stimulates Atg8 lipidation, autophagosome formation, and autophagic flux. It also induces transcriptional changes opposite to those observed in atg5 and atg7 mutants, favoring stress resistance and growth. As a result, ATG5- or ATG7-overexpressing plants exhibit increased resistance to necrotrophic pathogens and oxidative stress, delayed aging and enhanced growth, seed set, and seed oil content. This work provides an experimental paradigm and mechanistic insight into genetic stimulation of autophagy in planta and shows its efficiency for improving plant productivity.
Keywords	Arabidopsis ; autophagosomes ; autophagy ; disease resistance ; enzymes ; genetic suppression ; lipid content ; longevity ; mutants ; oxidative stress ; pathogens ; phenotype ; phosphatidylethanolamines ; seed oils ; seed set ; stress tolerance ; transcription (genetics)
Language	English
Dates of publication	2018-0314
Size	p. 1415-1432.
Publishing place	Oxford University Press
Document type	Article
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/ery010
Database	NAL-Catalogue (AGRICOLA)

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