Gibberellin Regulates Pollen Viability and Pollen Tube Growth in Rice

Bioscience and Biotechnology Center, Nagoya University, Chikusa, Nagoya 464-8601, Japan.
The Plant Cell (Impact Factor: 9.34). 01/2008; 19(12):3876-88. DOI: 10.1105/tpc.107.054759
Source: PubMed


Gibberellins (GAs) play many biological roles in higher plants. We collected and performed genetic analysis on rice (Oryza sativa) GA-related mutants, including GA-deficient and GA-insensitive mutants. Genetic analysis of the mutants revealed that rice GA-deficient mutations are not transmitted as Mendelian traits to the next generation following self-pollination of F1 heterozygous plants, although GA-insensitive mutations are transmitted normally. To understand these differences in transmission, we examined the effect of GA on microsporogenesis and pollen tube elongation in rice using new GA-deficient and GA-insensitive mutants that produce semifertile flowers. Phenotypic analysis revealed that the GA-deficient mutant reduced pollen elongation1 is defective in pollen tube elongation, resulting in a low fertilization frequency, whereas the GA-insensitive semidominant mutant Slr1-d3 is mainly defective in viable pollen production. Quantitative RT-PCR revealed that GA biosynthesis genes tested whose mutations are transmitted to the next generation at a lower frequency are preferentially expressed after meiosis during pollen development, but expression is absent or very low before the meiosis stage, whereas GA signal-related genes are actively expressed before meiosis. Based on these observations, we predict that the transmission of GA-signaling genes occurs in a sporophytic manner, since the protein products and/or mRNA transcripts of these genes may be introduced into pollen-carrying mutant alleles, whereas GA synthesis genes are transmitted in a gametophytic manner, since these genes are preferentially expressed after meiosis.

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    • "Similarly, the loss-of-function slr1-1 and the gain-of-function Slr1- d3 mutants exhibit sterile and semi-fertile phenotypes, respectively, in rice (Ikeda et al. 2001; Chhun et al. 2007). Although Slr1-d3 mutants produced normal floral organs with morphologically normal pistils and stamens, they showed low pollen viability compared to wild type, leading to semi-fertility in the Slr1-d3 mutants (Chhun et al. 2007). Our further phenotypic characterization showed that many agronomic traits related to yield and yield components were lower in HNIL(H143) compared with the EL1 HNIL(M23). "
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    ABSTRACT: Gibberellic acid (GA; or gibberellin) affects the development of floral organs, especially anthers and pollen, and perturbation of development of male floral organs can cause sterility. Many studies of GA signaling have concentrated on anther development, but the effect of GA on grain production remains to be examined. Using a cross of 'Milyang23 (M23)', which has a functional allele of Early flowering1 (EL1), and 'H143', which has a nonfunctional el1 allele, we generated heterogeneous inbred family-near isogenic lines (HNILs) that are homozygous for EL1 [HNIL(M23)] or el1 [HNIL(H143)]. Here, we found that HNIL(H143) exhibited anther deformities and low pollen viability. The expression of GAMYB, a major activator of GA signaling, and its downstream genes CYP703A3 and KAR, mainly involved in pollen formation, increased abnormally during spikelet development; this activation of GA signaling may cause the sterility. To confirm the negative effect of the el1 mutation on spikelet fertility, we examined a line carrying a T-DNA insertion el1 mutant [hereafter ZH11(el1)] and its parental cultivar 'Zhonghua11 (ZH11)'. ZH11(el1) showed nearly identical defects in anther development and pollen viability as HNIL(H143), leading to decreased seed setting rate. However, the elite japonica cultivar Koshihikari, which has a nonfunctional el1 allele for early flowering in long days, produces fertile spikelets and normal grain yields, like other elite japonica cultivars. This indicates that as-yet-unknown regulator(s) that can overcome the male sterile phenotype of the el1 mutation must have been introduced into Koshihikari. The el1 mutation contributes to early flowering in japonica rice under long days but fails to limit GA signaling, thus negatively affecting spikelet fertility, which results in a loss of grain yield. Thus, EL1 is essential for photoperiod sensitivity in flowering as well as spikelet fertility in grain production.
    Full-text · Article · Dec 2015 · Rice
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    • "Among the phytohormones, gibberellin (GA) is the most well known to be involved in controlling stem elongation, and a deficiency or insensitivity to GA could easily result in severe dwarfism as reported in many different kinds of plant species such as the rice mutants independently mutated in any of the six GA biosynthetic enzymes, ent-copalyl diphosphate synthase (CPS), ent-kaurene synthase (KS), ent-kaurene oxidase (KO), ent-kaurenoic acid oxidase (KAO), GA 20 oxidase (GA20ox), and GA 3-oxidase (GA3ox)22; the pea GA-deficient na-123; the Arabidopsis GA-insensitive short internodes (shi)24 and ga-insensitive (gai)25, and the GA-deficient ga1 – 3 mutants26; the barley GA-deficient grd2c mutant27, and the potato andigena (adg) mutant28. Across different species, GA-related mutants with severe dwarfism show several consensus phenotypes such as small dark-green leaves, delayed germination, defective flowering, reduced seed production and male sterility2228293031323334, whereas, semi-dwarf mutants only show mild height reduction with no adverse effects on overall morphology or agronomical traits. This is the reason why GA-related mutants with semi-dwarfism were widely used in the history of crop production. "
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    ABSTRACT: Regulation of symmetrical cell growth in the culm is important for proper culm development. So far, the involvement of gibberellin (GA) in this process has not yet been demonstrated in sorghum. Here, we show that GA deficiency resulting from any loss-of-function mutation in four genes (SbCPS1, SbKS1, SbKO1, SbKAO1) involved in the early steps of GA biosynthesis, not only results in severe dwarfism but also in abnormal culm bending. Histological analysis of the bent culm revealed that the intrinsic bending was due to an uneven cell proliferation between the lower and upper sides of culm internodes. GA treatment alleviated the bending and dwarfism in mutants, whereas the GA biosynthesis inhibitor, uniconazole, induced such phenotypes in wild-type plants- both in a concentration-dependent manner, indicating an important role of GA in controlling erectness of the sorghum culm. Finally, we propose that because of the tight relationship between GA deficiency-induced dwarfism and culm bending in sorghum, GA-related mutations have unlikely been selected in the history of sorghum breeding, as could be inferred from previous QTL and association studies on sorghum plant height that did not pinpoint GA-related genes.
    Full-text · Article · Jun 2014 · Scientific Reports
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    • "During inflorescence and fruit development, especially, the alteration of GA metabolism causes delay in floral development (Wilson et al. 1992), inhibition of stamen and pollen biogenesis (Goto and Pharis 1999; Hu et al. 2008; Plackett et al. 2011), inhibition of pollen tube growth (Chhun et al. 2007; Singh et al. 2002), seed abortion (Singh C. J. Jung and Y. Y. Hur contributed equally to this work. "
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    ABSTRACT: The concept that gibberellin (GA) application on seeded grapevines induces seedlessness has been known for decades in viticulture. GA was applied to inflorescence clusters of seeded diploid grapevine cultivar ‘Tamnara’ (Vitis spp.) at 14 days before full bloom (DBF). Morphological and molecular effects of GA application were examined on the induction of parthenocarpic fruit development. With GA application, ovaries were enlarged and pollen tube growth was completely inhibited. Vitis GA oxidase enzymes, key determinants for GA level, were characterized through phylogenetic analysis with Arabidopsis GA oxidase enzymes. Five VvGA 20-oxidase (VvGA20ox), three VvGA 3-oxidase (VvGA3ox), and nine VvGA 2-oxidase (VvGA2ox) family proteins, and one VvGA methyltransferase (VvGAMT) and one Vitis cytochrome P450 714A1 proteins were identified, and their expression patterns were analyzed during inflorescence development from 14 DBF to 5 days after full bloom (DAF). VvGA2ox1, VvGA20ox3, and VvGA3ox2 were the most abundantly expressed genes in each gene family at 7, 5, and 2 DBF, respectively. Following GA application at 14 DBF inducing seedlessness, GA catabolic genes such as VvGAMT2, VvGA2ox3, and VvGA2ox4 were up-regulated at 12 DBF, full bloom, and 5 DAF, respectively. Conversely, most GA biosynthetic genes, VvGA20oxs and VvGA3oxs, were down-regulated at near full bloom, and the timing of their peak expression was changed. These results suggest that GA application at pre-bloom changes the GA biosynthesis into GA catabolic pathway at near full bloom by altering the transcription level and timing of GA oxidase genes during grapevine inflorescence development.
    Full-text · Article · Dec 2013 · Journal of Plant Research
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