Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation

Varnier, Anne-Lise; Mazeyrat-Gourbeyre, Florence; Sangwan, Rajbir S.; Clément, Christophe

doi:10.1016/j.jsb.2005.07.011

Cited by 107 publications

(89 citation statements)

References 42 publications

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“…Plants were grown as described earlier (Jacquard et al 2003(Jacquard et al , 2006. Spikes were collected when the microspores were at the mid-uninucleate stage (Szarejko 2003), which was determined using Hoechst 33342 nuclear staining according to Varnier et al (2005). We followed expression of stress-related genes during in vivo development and in vitro during the stress treatment.…”

Section: Methodsmentioning

confidence: 99%

Microspore embryogenesis in barley: anther pre-treatment stimulates plant defence gene expression

Jacquard

Mazeyrat-Gourbeyre

Devaux³

et al. 2008

Planta

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Microspore embryogenesis (ME) is a process in which the gametophytic pollen programme of the microspore is reorientated towards a new embryo sporophytic programme. This process requires a stress treatment, usually performed in the anther or isolated microspores for several days. Despite the universal use of stress to induce ME, very few studies have addressed the physiological processes that occur in the anther during this step. To further understand the processes triggered by stress treatment, we followed the response of anthers by measuring the expression of stressrelated genes in two barley (Hordeum vulgare L.) cultivars differing in their ME response. Genes encoding enzymes involved in oxidative stress (glutathione-S-transferase, GST; oxalate oxidase, OxO), in the synthesis of jasmonic acid (13-lipoxygenase, Lox; allene oxide cyclase, AOC; allene oxide synthase, AOS) and in the phenylpropanoid pathway (phenylalanine ammonia lyase, PAL), as well as those encoding PR proteins (Barwin, chitinase 2b, Chit 2b; glucanase, Gluc; basic pathogenesis-related protein 1, PR1; pathogenesis-related protein 10, PR10) were up-regulated in whole anthers upon stress treatment, indicating that anther perceives stress and reacts by triggering general plant defence mechanisms. In particular, both OxO and Chit 2b genes are good markers of anther reactivity owing to their high level of induction during the stress treatment. The effect of copper sulphate appeared to limit the expression of defence-related genes, which may be correlated with its positive effect on the yield of microspore embryos.

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Section: Methodsmentioning

confidence: 99%

Microspore embryogenesis in barley: anther pre-treatment stimulates plant defence gene expression

Jacquard

Mazeyrat-Gourbeyre

Devaux³

et al. 2008

Planta

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“…Bars = 20 mm in (A) to (C), 50 mm in (G), and 10 mm in (H) and (I). (Papini et al, 1999;Varnier et al, 2005;Li et al, 2006). Tapetal cell differentiation and disintegration coincide with the postmeiotic developmental program, and premature or delayed degradation of the tapetum is associated with male sterility.…”

Section: Mads3 Regulates Ros Homeostasis During Anther Developmentmentioning

confidence: 99%

Rice MADS3 Regulates ROS Homeostasis during Late Anther Development

et al. 2011

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The rice (Oryza sativa) floral homeotic C-class gene, MADS3, was previously shown to be required for stamen identity determination during early flower development. Here, we describe a role for MADS3 in regulating late anther development and pollen formation. Consistent with this role, MADS3 is highly expressed in the tapetum and microspores during late anther development, and a newly identified MADS3 mutant allele, mads3-4, displays defective anther walls, aborted microspores, and complete male sterility. During late anther development, mads3-4 exhibits oxidative stress-related phenotypes. Microarray analysis revealed expression level changes in many genes in mads3-4 anthers. Some of these genes encode proteins involved in reactive oxygen species (ROS) homeostasis; among them is MT-1-4b, which encodes a type 1 small Cys-rich and metal binding protein. In vivo and in vitro assays showed that MADS3 is associated with the promoter of MT-1-4b, and recombinant MT-1-4b has superoxide anion and hydroxyl radical scavenging activity. Reducing the expression of MT-1-4b causes decreased pollen fertility and an increased level of superoxide anion in transgenic plants. Our findings suggest that MADS3 is a key transcriptional regulator that functions in rice male reproductive development, at least in part, by modulating ROS levels through MT-1-4b.

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“…Tapetum degradation is considered to be a process of programmed cell death (PCD; Papini et al, 1999;Wu and Cheung, 2000). Its typical cytological features, including cytoplasmic shrinkage, oligonucleosomal cleavage of DNA, vacuole rupture, and swelling of the endoplasmic reticulum, during tapetum development in angiosperms have been characterized (Papini et al, 1999;Varnier et al, 2005;Li et al, 2006). Abnormalities in tapetal degeneration usually cause male sterility in plants.…”

Section: Introductionmentioning

confidence: 99%

Rice APOPTOSIS INHIBITOR5 Coupled with Two DEAD-Box Adenosine 5′-Triphosphate-Dependent RNA Helicases Regulates Tapetum Degeneration

et al. 2011

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Programmed cell death (PCD) during tapetum degeneration in postmeiotic anthers is critical for the proper development of male gametophytes in flowering plants. Although several genes involved in this process have been identified recently, the molecular mechanism is still poorly understood. Here, we show that knockout of rice (Oryza sativa) APOPTOSIS INHIBITOR5 (API5), which encodes a putative homolog of antiapoptosis protein Api5 in animals, results in delayed degeneration of the tapetum due to inhibition of the tapetal PCD process leading to defects in formation of male gametophytes. Os API5 is a nuclear protein that interacts with two DEAD-box ATP-dependent RNA helicases, API5-INTERACTING PROTEIN1 (AIP1) and AIP2. AIP1 and AIP2 are homologs of yeast (Saccharomyces cerevisiae) Suppressor of Bad Response to Refrigeration1 protein 2 (SUB2p) that have critical roles in transcription elongation and pre-mRNA splicing. Os AIP1 and AIP2 can form dimers and interact directly with the promoter region of CP1, a rice cysteine protease gene. Suppression of Os AIP1/2 leads to downregulation of CP1, resulting in sterility, which is highly similar to the effects of suppressed expression of Os CP1. Our results uncover a previously unknown pathway for regulating PCD during tapetum degeneration in rice, one that may be conserved among eukaryotic organisms.

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Programmed cell death progressively models the development of anther sporophytic tissues from the tapetum and is triggered in pollen grains during maturation

Cited by 107 publications

References 42 publications

Microspore embryogenesis in barley: anther pre-treatment stimulates plant defence gene expression

Microspore embryogenesis in barley: anther pre-treatment stimulates plant defence gene expression

Rice MADS3 Regulates ROS Homeostasis during Late Anther Development

Rice APOPTOSIS INHIBITOR5 Coupled with Two DEAD-Box Adenosine 5′-Triphosphate-Dependent RNA Helicases Regulates Tapetum Degeneration

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