Comprehensive Insight into Gibberellin- and Jasmonate-Mediated Stamen Development
Abstract
:1. Introduction
2. Structure, Function and Development of Stamens
3. Gibberellin-Mediated Stamen Development and Functioning
3.1. GA Biosynthesis Is Crucial for Correct Stamen Development and Functioning in Various Plants
3.1.1. GA Biosynthesis Pathway—General Information
3.1.2. Early Stages of GA Biosynthesis
3.1.3. Late Stages of GA Biosynthesis
3.2. Perception, Signal Transduction and Action of GAs during Stamen Development
3.2.1. GA Signaling Pathway—General Information
3.2.2. Receptor—Dependent Signaling
3.2.3. The Role of DELLA Proteins
3.2.4. Events Downstream of DELLAs during Filament Elongation and Anther Development
4. Jasmonate-Dependent Stamen Development and Functioning
4.1. The Importance of JA Biosynthesis in Proper Stamen Development
4.1.1. JA Metabolism—General Information
4.1.2. Studies on JA Biosynthesis Mutants
4.2. Perception, Signal Transduction and Action of JAs during Stamen Development
4.2.1. JA Signaling Pathway—General Information
4.2.2. JA Signaling Dependent on the COI Receptor
4.2.3. The Pathway Downstream of the JAZ Repressor
5. Gibberellin-Jasmonate Interactions in the Regulation of Stamen Development
6. Hormonal Transport in Stamen Development
7. Summary
Author Contributions
Funding
Conflicts of Interest
References
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Gene | Mutant | Phenotype | Species | Refs |
---|---|---|---|---|
AtCPS | ga1-3 | Male-sterile phenotype, which can be reversed by GA application | Arabidopsis | [40] |
Anther and pollen development is blocked after meiosis but prior to mitosis | ||||
Pollen sacs expansion arrest | ||||
Inability to release microspores | ||||
Tapetum remains at the vacuolated stage and degenerates together with the microspores | ||||
Inhibition of filament elongation by a reduction of the length, not the number of cells | ||||
Altered ratio of stamen-pistil length in the flowers of mature mutant | ||||
LeCPS | gib-1 | Initiation of floral meristems and development of all floral organs proceeds normally up to a certain point, but then normal development ceases and flower buds eventually abort | tomato | [47] |
Microsporogenesis is blocked before meiosis | ||||
Anthers of developmentally arrested buds contain PMCs that are in the G1 phase of premeiotic interphase. Following treatment of mutant buds with GA3, premeiotic DNA synthesis and callose accumulation in PMCs are evident by 48 h posttreatment, and within 66 h, prophase I of meiosis and meiosis-related changes in tapetum development are observable | ||||
OsCPS1 | oscps1-1 | One of the most severe GA-deficient mutant | rice | [48] |
GA treatment rescues the defect in stamen development | ||||
Abnormal enlargement of tapetal cells, to the point of almost filling the locule space | ||||
Collapse of microspores | ||||
LeKAO | ga-2 | Flower buds are initiated, but do not develop to maturity and eventually abort | tomato | [39] |
Cells of the sporogenous layer are initiated, but growth is arrested and cells eventually degenerate | ||||
Inhibition of microsporogenesis occurs before meiosis | ||||
Stamen do not elongate | ||||
OsKAO | rpe1 | Intermediate severity GA-deficient mutant | rice | [49] |
The mutant develops typical flowers with normal pistils and stamens | ||||
Pollen viability and the number of mature pollen grains in mutant are similar to those of the WT plant | ||||
Impaired pollen germination and elongation | ||||
GA20ox | ga20ox1 ga20ox2 | Semidwarf, semifertile phenotype, with early flowers failing to set seed | Arabidopsis | [37] |
Self-rescue of seed set occurs in later flowers, although the mechanism remains undetermined | ||||
Normal tapetum degradation | ||||
Fully viable pollen | ||||
Delayed or inhibited anther dehiscence | ||||
Disturbance of filament elongation | ||||
ga20ox1 ga20ox2 ga20ox3-1 | For many phenotypic characters, the triple mutant is not significantly different from the ga1-3 | [53] | ||
Postmeiotic arrest in stamen development | ||||
Defect in tapetum degeneration. Tapetum layer fails to degenerate completely and remains in anther locules | ||||
Inhibited anther dehiscence | ||||
Do not undergo late-stage stamen acceleration, with growth and development instead halting | ||||
Shorter stamens at flower opening | ||||
GA3ox | ga3ox1 ga3ox3 | The epidermal layer of the anther remains intact, although the tapetum layer disappears, suggesting that anther development is arrested around stages 11 and 12 | Arabidopsis | [36] |
Defective pollen after its maturation | ||||
Delayed or inhibited anther dehiscence | ||||
Disturbances in filament elongation | ||||
All defects gradually decrease in the later flowers |
Gene | Mutant | Phenotype | Species | Refs |
---|---|---|---|---|
AtGID1 | gid1a-1 gid1b-1 gid1c-1 | Complete infertility and unresponsiveness to GA treatment | Arabidopsis | [35] |
The triple mutant exhibits more pronounced disturbances in stamen development than ga1-3 | ||||
Anther development in this mutant has not been described | ||||
Dramatic reduction in length of filaments | ||||
OsGID1 | gid1-4 | Anther-wide developmental arrest to occur either just prior to or during meiosis | rice | [48] |
PMCs are condensed and do not form tetrads | ||||
Abnormal stamens with shrunken and whitened anthers | ||||
Slightly enlarged tapetal cells that nearly fill the locule and contain the degraded meiocyte | ||||
Middle layer of cells does not degrade | ||||
Failure in epidermal cell expansion | ||||
GAI RGA RGL1 RGL2 | ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 | Penta mutant can produce fully developed fertile flowers as the WT control | Arabidopsis | [40] |
ga1-3 gai-t6 rgl1-1 rgl2-1 ga1-3 gai-t6 rgl1-1 rga-t2 | Those quadruple mutants with expression of only RGA or RGL2 are completely sterile | |||
Mutants are effective in inhibiting the expression of MYB21, MYB24 and MYB57 | ||||
ga1-3 rga-t2 rgl1-1 rgl2-1 ga1-3 gai-t6 rga-t2 rgl2-1 | Those quadruple mutants with expression of only GAI or RGL1 are fully fertile | |||
Mutants are ineffective in inhibiting the expression of MYB21, MYB24 and MYB57 | ||||
SLR1 | Slr1-d3 | Constitutive GA responce mutant is semifertile, even though it develops normal flowers with morphologically normal stamens and pistils | rice | [49] |
The anthers appear normal and produce a similar number of pollen grains as WT plants | ||||
High frequency of nonviable pollen | ||||
slr1-1 | Sterile phenotype | [59] | ||
Impaired floral development | ||||
SLN1 | sln | Infertility due to impaired floral development | barley | [60] |
MYB21 MYB24 MYB57 | myb21-t1 myb24-t1 myb57-t1 | Pollen is partial viable | Arabidopsis | [67] |
Short stamens are the main cause of the mutant sterility | ||||
MYB33 MYB65 | myb33 myb65 | Anthers are smaller than those in the WT plants and fail to produce pollen. The block in pollen development appears to be premeiotic occurring between anther stages 5 and 6 | Arabidopsis | [70] |
During sixth stage of anther development when the PMCs begin to separate in a clearly defined locule and the tapetum begins to vacuolate, the mutant is similar, except that the tapetum begins to enlarge. Next, the tapetum expand to such an extent that there is no locule, and the PMCs have an irregular shape. Whereas microspores form in the locule of WT anthers and eventually form mature pollen, the tapetum of the mutant continues to expand until the contents collapse and degenerate. The expansion of the tapetum appears to be due to an increase in cell size, not in cell number | ||||
Stamens shorter than their WT counterparts and fail to fully extend to the pistil | ||||
Other than sterility and the associated characteristics of sterile plants, mutant shows no obvious morphological differences from WT plants |
Gene | Mutant | Phenotype | Species | Refs |
---|---|---|---|---|
PLA1/ DAD1 | dad1 | WT phenotype can be rescued by the JA application | Arabidopsis | [76] |
Developmental delay of flower bud opening | ||||
Before flower opening, all cell types are normally developed in mutant anthers, similar to all structural features | ||||
Pollen grains develop normally up to the trinucleate stage | ||||
A defect in pollen grains occurs at the final stage of their maturation | ||||
Defective in anther dehiscence | ||||
P0491E01 | Normal anther development at the initial stages | rice | [81] | |
Microspores development into mature pollen grains is impaired | ||||
LOX3 LOX4 | lox3 lox4 | Male sterile. JA application restored fertility | Arabidopsis | [82] |
Abnormal anther maturation | ||||
Pollen is not viable | ||||
Defective dehiscence | ||||
Shorter filaments | ||||
AOS | dde2-2 | Male-sterile phenotype which can be rescued by Me-JA application | Arabidopsis | [83] |
Impaired anther dehiscence and filament elongation | ||||
DDE1/ OPR3 | dde1/opr3 | WT phenotype can be rescued by the MeJA application | Arabidopsis | [84,85] |
Floral organs develop normally within the closed bud | ||||
The anther locules do not dehisce at the time of flower opening | ||||
Pollen develops to the trinucleate stage | ||||
Pollen grains are predominantly inviable | ||||
The filaments do not elongate sufficiently to position the locules above the stigma at anthesis |
Gene | Mutant | Phenotype | Species | Refs |
---|---|---|---|---|
COI1 | coi-1 | Delayed anther dehiscence | Arabidopsis | [101,102] |
Reduced pollen viability in the 13th phase of flower development | ||||
Abnormal filament elongation | ||||
MYC2 MYC3 MYC4 MYC5 | myc2 myc3 myc4 myc5 | Pollen grains do not germinate in vitro | [94] | |
The anthers dehisce and release viable pollen at floral stage 15 | ||||
The filament does not elongate normally at floral stage 13 | ||||
MYB21 MYB24 | myb21 myb24 | Greatly reduced male fertility. Restore the WT phenotype via JA application | [91] | |
Delayed anther dehiscence | ||||
Very short filaments | ||||
MYB108 | myb108 | Reduced male fertility | [93] | |
Delayed anther dehiscence | ||||
Reduced pollen viability |
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Marciniak, K.; Przedniczek, K. Comprehensive Insight into Gibberellin- and Jasmonate-Mediated Stamen Development. Genes 2019, 10, 811. https://doi.org/10.3390/genes10100811
Marciniak K, Przedniczek K. Comprehensive Insight into Gibberellin- and Jasmonate-Mediated Stamen Development. Genes. 2019; 10(10):811. https://doi.org/10.3390/genes10100811
Chicago/Turabian StyleMarciniak, Katarzyna, and Krzysztof Przedniczek. 2019. "Comprehensive Insight into Gibberellin- and Jasmonate-Mediated Stamen Development" Genes 10, no. 10: 811. https://doi.org/10.3390/genes10100811