Ultrastructural study of rice tapetum under low-temperature stress
TL;DR: Cytological observations of the anther showed that the tapetum was the most sensitive to low-temperature stress, resulting in male sterility due to functional loss of the tissue, and this abnormality was restricted primarily to the ER structures.
Abstract: The development of male reproductive organs in rice is very sensitive to various environmental stresses. For example, exposing plants to low temperatures during the heading stage leads to a reduction in grain yield. Here, we grew rice under normal conditions and also at three different temperatures -- 16, 18, and 20°C. Treatment at a low temperature significantly decreased pollen viability and grain production. Cytological observations of the anther showed that the tapetum was the most sensitive to low-temperature stress, resulting in male sterility due to functional loss of the tissue. Detailed observations by transmission electron microscopy suggested that this abnormality was restricted primarily to the ER structures. The endoplasmic reticulum, a highly vulnerable sub-cellular organelle, showed two typical morphological aberrations, one in its pattern of arrangement, the other in the formation of ER bodies. Of our three experimental chilling temperatures, the most severe abnormalities were observed in tapetal cells exposed to 16°C.
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TL;DR: This review presents the critically stress-sensitive stages of male sporogenesis (meiosis) and male gametogenesis (microspore development), and discusses the corresponding biological processes involved and the resulting alterations in male reproduction.
Abstract: In plants, male reproductive development is extremely sensitive to adverse climatic environments and (a)biotic stress. Upon exposure to stress, male gametophytic organs often show morphological, structural and metabolic alterations that typically lead to meiotic defects or premature spore abortion and male reproductive sterility. Depending on the type of stress involved (e.g. heat, cold, drought) and the duration of stress exposure, the underlying cellular defect is highly variable and either involves cytoskeletal alterations, tapetal irregularities, altered sugar utilization, aberrations in auxin metabolism, accumulation of reactive oxygen species (ROS; oxidative stress) or the ectopic induction of programmed cell death (PCD). In this review, we present the critically stress-sensitive stages of male sporogenesis (meiosis) and male gametogenesis (microspore development), and discuss the corresponding biological processes involved and the resulting alterations in male reproduction. In addition, this review also provides insights into the molecular and/or hormonal regulation of the environmental stress sensitivity of male reproduction and outlines putative interaction(s) between the different processes involved.
327 citations
TL;DR: A better understanding of the physiological and molecular processes that lead to stress-induced pollen abortion may provide the key to finding solutions for maintaining grain number under abiotic stress conditions.
281 citations
Cites background from "Ultrastructural study of rice tapet..."
...Both cold and drought stress have been shown to cause a pre-mature cell death response in the tapetum [44, 45], suggesting that abiotic stress interferes with the important functions of the tapetum....
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...Subsequently, a premature cell death response is observed in the tapetum of sensitive varieties, leading to abortion of pollen development [44, 45]....
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TL;DR: The data indicate that ABA and ABA 8′-hydroxylase play an important role in controlling anther ABA homeostasis and reproductive stage abiotic stress tolerance in cereals.
Abstract: Drought stress at the reproductive stage causes pollen sterility and grain loss in wheat (Triticum aestivum). Drought stress induces abscisic acid (ABA) biosynthesis genes in anthers and ABA accumulation in spikes of drought-sensitive wheat varieties. In contrast, drought-tolerant wheat accumulates lower ABA levels, which correlates with lower ABA biosynthesis and higher ABA catabolic gene expression (ABA 8'-hydroxylase). Wheat TaABA8'OH1 deletion lines accumulate higher spike ABA levels and are more drought sensitive. ABA treatment of the spike mimics the effect of drought, causing high levels of sterility. ABA treatment represses the anther cell wall invertase gene TaIVR1, and drought-tolerant lines appeared to be more sensitive to the effect of ABA. Drought-induced sterility shows similarity to cold-induced sterility in rice (Oryza sativa). In cold-stressed rice, the rate of ABA accumulation was similar in cold-sensitive and cold-tolerant lines during the first 8 h of cold treatment, but in the tolerant line, ABA catabolism reduced ABA levels between 8 and 16 h of cold treatment. The ABA biosynthesis gene encoding 9-cis-epoxycarotenoid dioxygenase in anthers is mainly expressed in parenchyma cells surrounding the vascular bundle of the anther. Transgenic rice lines expressing the wheat TaABA8'OH1 gene under the control of the OsG6B tapetum-specific promoter resulted in reduced anther ABA levels under cold conditions. The transgenic lines showed that anther sink strength (OsINV4) was maintained under cold conditions and that this correlated with improved cold stress tolerance. Our data indicate that ABA and ABA 8'-hydroxylase play an important role in controlling anther ABA homeostasis and reproductive stage abiotic stress tolerance in cereals.
245 citations
Cites background from "Ultrastructural study of rice tapet..."
...Both cold and drought stresses were shown to trigger a premature cell death response in the tapetum (Oliver et al., 2005; Gothandam et al., 2007; Nguyen et al., 2009; Ji et al., 2010)....
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TL;DR: In this article, the effects of low and high-temperature sensitivity in rice at various reproductive stages (from meiosis to grain development) and propose strategies for improving the tolerance of rice to terminal thermal stress.
134 citations
TL;DR: Improving cereal productivity will be a matter of increasing yield potential of current germplasm, but also of improving yield stability through enhanced tolerance to abiotic stresses in a world with a changing climate.
Abstract: The United Nations Food and Agriculture Organisation (FAO) forecasts a 34% increase in the world population by 2050. As a consequence, the productivity of important staple crops such as cereals needs to be boosted by an estimated 43%. This growth in cereal productivity will need to occur in a world with a changing climate, where more frequent weather extremes will impact on grain productivity. Improving cereal productivity will, therefore, not only be a matter of increasing yield potential of current germplasm, but also of improving yield stability through enhanced tolerance to abiotic stresses. Successful reproductive development in cereals is essential for grain productivity and environmental constraints (drought, cold, frost, heat and waterlogging) that are associated with climate change are likely to have severe effects on yield stability of cereal crops. Currently, genetic gains conferring improved abiotic stress tolerance in cereals is hampered by the lack of reliable screening methods, availability of suitable germplasm and poor knowledge about the physiological and molecular underpinnings of abiotic stress tolerance traits.
123 citations
Cites background from "Ultrastructural study of rice tapet..."
...Cold stress in rice was shown to primarily affect the endoplasmatic reticulum (ER) in the tapetum layer (Gothandam et al. 2007)....
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References
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TL;DR: Reproductive development of plants is highly vulnerable to water deficit, and changes in carbohydrate availability and metabolism appear to be involved in the effects of stress during meiosis and anthesis, which can cause loss of pollen fertility, failure of pollination, spikelet death, or zygotic abortion.
Abstract: Reproductive development of plants is highly vulnerable to water deficit. Stress early during this phase can delay or completely inhibit flowering, both through an inhibition of floral induction and development. The stage of meiosis is perhaps the most stress-sensitive period of reproduction in all species studied. A meiotic-stage water deficit causes pollen sterility, but usually affects female fertility only under extreme stress. Sterility occurs even though the reproductive structures of stressed plants maintain a high water status, indicating that the response is probably mediated by a sporocidal signal from elsewhere in the plant. Rice and maize plants are also highly vulnerable during flowering (anthesis) and early grain initiation. Stress during this period can cause loss of pollen fertility, failure of pollination, spikelet death, or zygotic abortion. Changes in carbohydrate availability and metabolism appear to be involved in the effects of stress during meiosis and anthesis. Stress during early grain development curtails the kernel sink potential by reducing the number of endosperm cells and amyloplasts formed. Controls underlying these effects are poorly understood, although hormones may be involved. A water deficit during any stage of grain development causes the premature cessation of grain filling. Kernel moisture content and its direct impact on metabolism appear to be key regulatory factors in shortening the duration of grain filling.
563 citations
"Ultrastructural study of rice tapet..." refers background in this paper
...The reproductive stage is particularly sensitive to abiotic stress (e.g., from cold, drought, or heat) not only in rice but also in other cereal crops (Saini and Westgate, 2000; Boyer and Westgate, 2004)....
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TL;DR: The ovary rescue with sucrose feeding indicates either that the changes identified in the profiling are of no consequence for inhibiting ovary development or that gene expression reverts to control levels when the sugar stream recovers.
Abstract: Plant reproduction is sensitive to water deficits, especially during the early phases when development may cease irreversibly even though the parent remains alive. Grain numbers decrease because of several developmental changes, especially ovary abortion in maize (Zea mays L.) or pollen sterility in small grains. In maize, the water deficits inhibit photosynthesis, and the decrease in photosynthate flux to the developing organs appears to trigger abortion. Abscisic acid also increases in the parent and may play a role, perhaps by inhibiting photosynthesis through stomatal closure. Recent work indicates that invertase activity is inhibited and starch is diminished in the ovaries or affected pollen. Also, sucrose fed to the stems rescues many of the ovaries otherwise destined to abort. The feeding restores some of the ovary starch and invertase activity. These studies implicate invertase as a limiting enzyme step for grain yields during a water deficit, and transcript profiling with microarrays has identified genes that are up- or down-regulated during water deficit-induced abortion in maize. However, profiling studies to date have not reported changes in invertase or starch synthesizing genes in water-deficient ovaries, perhaps because there were too few sampling times. The ovary rescue with sucrose feeding indicates either that the changes identified in the profiling are of no consequence for inhibiting ovary development or that gene expression reverts to control levels when the sugar stream recovers. Careful documentation of tissue- and developmentally specific gene expression are needed to resolve these issues and link metabolic changes to the decreased sugar flux affecting the reproductive organs.
397 citations
"Ultrastructural study of rice tapet..." refers background in this paper
...The reproductive stage is particularly sensitive to abiotic stress (e.g., from cold, drought, or heat) not only in rice but also in other cereal crops (Saini and Westgate, 2000; Boyer and Westgate, 2004)....
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TL;DR: AMS plays a crucial role in tapetal cell development and the post-meiotic transcriptional regulation of microspore development within the developing anther in Arabidopsis thaliana.
Abstract: Visual screening of a T-DNA mutagenised population of Arabidopsis thaliana for an absence of silique elongation lead to the isolation of the aborted microspores (ams) mutant that shows a sporophytic recessive male sterile phenotype. Homozygous mutant plants are completely devoid of mature pollen. Pollen degeneration occurs shortly after release of the microspores from the tetrad, prior to pollen mitosis I. Premature tapetum and microspore degeneration are the primary defects caused by this lesion, while a secondary effect is visualised in the stamen filaments, which are reduced in length and lie beneath the receptive stigma at flower opening. The disrupted gene was isolated and revealed a T-DNA element to be inserted into the eighth exon of a basic helix-loop-helix (bHLH) gene located on chromosome II. This protein sequence contains a basic DNA binding domain and two alpha helices separated by a loop, typical of a transcription factor belonging to the MYC sub family of bHLH genes. Therefore, AMS plays a crucial role in tapetal cell development and the post-meiotic transcriptional regulation of microspore development within the developing anther.
377 citations
"Ultrastructural study of rice tapet..." refers background in this paper
...…as early degeneration, hypertrophy, or mutations in the archesporial cell) lead to aborted microgametogenesis and male sterility (Chaudhury, 1993; Wilson et al., 2001; Kapoor et al., 2002; Sorensen et al., 2002, 2003; Higginson et al., 2003; Jung et al., 2005; Oliver et al., 2005; Wi et al., 2005)....
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TL;DR: The deduced MS1 protein sequence shows strong homology to the PHD-finger motif found in known transcription factors from humans, yeast and higher plants, and is likely to play a key role in regulating transcription during specific stages of male gametogenesis and anther development.
Abstract: We report here the molecular characterisation of the Arabidopsis MALE STERILITY1 gene, which is a critical sporophytic controlling factor for anther and pollen development. Homozygous ms1 mutants do not produce viable pollen, but are otherwise phenotypically normal. Degeneration of pollen occurs soon after microspore release from the tetrads, at which time the tapetum also appears abnormally vacuolated. The MS1 gene is expressed at low levels in anthers from closed buds, with expression in the tapetum at the stage of microspore release. No expression is seen in open flowers. The deduced MS1 protein sequence shows strong homology to the PHD-finger motif found in known transcription factors from humans, yeast and higher plants. Six alleles of ms1 have been identified; all result in premature termination of the MS1 protein and loss of the PHD-finger motif. MS1 is likely to play a key role in regulating transcription during specific stages of male gametogenesis and anther development. As such, MS1 provides a valuable tool for the manipulation of male sterility in higher plants.
354 citations
TL;DR: A hypothetical phylogenesis of the tapetum is proposed on the basis of its morphological appearance and of the nutritional relations with meiocytes/spores, and the evolutionary trends of thetapeta tend towards a more and more intimate and increasingly greater contact with the spores/pollen grains.
Abstract: It appears that the tapetum is universally present in land plants, even though it is sometimes difficult to recognize, because it serves mostly as a tissue for meiocyte/spore nutrition. In addition to this main function, the tapetum has other functions, namely the production of the locular fluid, the production and release of callase, the conveying of P.A.S. positive material towards the loculus, the formation of exine precursors, viscin threads and orbicules (= Ubisch bodies), the production of sporophytic proteins and enzymes, and of pollenkitt/tryphine. Not all these functions are present in all land plants:Embryophyta. Two main tapetal types are usually distinguished in theSpermatophyta: the secretory or parietal type and the amoeboid or periplasmodial type; in lower groups, however, other types may be recognized, with greater or lesser differences. A hypothetical phylogenesis of the tapetum is proposed on the basis of its morphological appearance and of the nutritional relations with meiocytes/spores. The evolutionary trends of the tapeta tend towards a more and more intimate and increasingly greater contact with the spores/pollen grains. Three evolutionary trends can be recognized: 1) an intrusion of the tapetal cells between the spores, 2) a loss of tapetal cell walls, and 3) increasing nutrition through direct contact in narrow anthers.
346 citations
"Ultrastructural study of rice tapet..." refers background in this paper
...The tapetum is a highly specialized secretory cell layer responsible both for pollen cell wall deposition and for the production of locular fluid that supplies the nutrients required for pollen maturation (Steer, 1977; Pacini et al., 1985; Clement et al., 1994, 1998)....
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...Plasmodesmata between the tapetum and the outer cell layers of the anther wall disappear at meiosis, and callose deposition isolates the meiocytes from the rest of the anther (Steer, 1977; Pacini and Franchi, 1983; Pacini et al., 1985; Raghavan, 1988; Clement and Audran, 1995)....
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