A Rice Ca<sup>2+</sup> Binding Protein Is Required for Tapetum Function and Pollen Formation

Yu, Jing; Meng, Zhaolu; Liang, Wanqi; Behera, Smrutisanjita; Kudla, Jörg; Tucker, Matthew R.; Luo, Zhijing; Chen, Mingjiao; Xu, Dawei; Zhao, Guochao; Wang, Jie; Zhang, Siyi; Kim, Yujin; Zhang, Dabing

doi:10.1104/pp.16.01261

Cited by 53 publications

(53 citation statements)

References 93 publications

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“…Primer sequences used for amplification are shown in Table S3. In situ hybridization was performed according to Yu et al .…”

Section: Methodsmentioning

confidence: 99%

The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice

Zhu

Shi

et al. 2017

JIPB

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Lipid and phenolic metabolism are important for pollen exine formation. In Arabidopsis, polyketide synthases (PKSs) are essential for both sporopollenin biosynthesis and exine formation. Here, we characterized the role of a polyketide synthase (OsPKS2) in male reproduction of rice (Oryza sativa). Recombinant OsPKS2 catalyzed the condensation of fatty acyl-CoA with malonylCoA to generate triketide and tetraketide a-pyrones, the main components of pollen exine. Indeed, the ospks2 mutant had defective exine patterning and was male sterile. However, the mutant showed no significant reduction in sporopollenin accumulation. Compared with the WT (wild type), ospks2 displayed unconfined and amorphous tectum and nexine layers in the exine, and less organized Ubisch bodies. Like the pksb/lap5 mutant of the Arabidopsis ortholog, ospks2 showed broad alterations in the profiles of anther-related phenolic compounds. However, unlike pksb/lap5, in which most detected phenolics were substantially decreased, ospks2 accumulated higher levels of phenolics. Based on these results and our observation that OsPKS2 is unable to fully restore the exine defects in the pksb/lap5, we propose that PKS proteins have functionally diversified during evolution. Collectively, our results suggest that PKSs represent a conserved and diversified biochemical pathway for anther and pollen development in higher plants.

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“…Primer sequences used for amplification are shown in Table S3. In situ hybridization was performed according to Yu et al .…”

Section: Methodsmentioning

confidence: 99%

The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice

Zhu

Shi

et al. 2017

JIPB

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“…MS26 encodes a cytochrome P450 monooxygenase and was found to function in the fatty acid metabolism pathway. Similarly, many tapetum‐expressed genes which are involved in fatty acid metabolism and lipid transporters are well known in rice, including WAX‐DEFICIENT ANTHER1 ( WDA1 ) (Jung et al ., ), DEFECTIVE POLLEN WALL ( DPW ) (Shi et al ., ), DPW2 (Xu et al ., ), CYP704B2 (Li et al ., ), POST‐MEIOTIC DEFICIENT ANTHER1 ( PDA1 ) (Hu et al ., ), CYP703A3 (Yang et al ., ), TAPETUM DEGENERATION RETARDATION ( TDR ) (Li et al ., ), DEFECTIVE TAPETUM CELL DEATH 1 ( DTC1 ) (Yi et al ., ), OsDEX1 (Yu et al ., ), OsC6 (Zhang et al ., ), OsABCG15 (Wu et al ., ), OsABCG26 (Zhao et al ., ), and MALE STERILITY2 ( MS2 ) (Chen et al ., ; Doan et al ., ), CYP704B1 (Dobritsa et al ., ), CYP703A2 (Morant et al ., ), Acyl‐CoA Synthetase ( ACOS5 ) (de Azevedo Souza et al ., ), and AtSEC31B (Zhao et al ., ) in Arabidopsis. The rice cyp703a3 mutant displays complete male sterility, whereas its Arabidopsis orthologous cyp703a2 mutant produces partially sterile pollen grains that display an abnormal exine with no obvious sporopollenin deposition.…”

Section: Introductionmentioning

confidence: 99%

ABNORMAL POLLEN VACUOLATION1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize

et al. 2017

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Anther cuticle and pollen exine are the major protective barriers against various stresses. The proper functioning of genes expressed in the tapetum is vital for the development of pollen exine and anther cuticle. In this study, we report a tapetum-specific gene, Abnormal Pollen Vacuolation1 (APV1), in maize that affects anther cuticle and pollen exine formation. The apv1 mutant was completely male sterile. Its microspores were swollen, less vacuolated, with a flat and empty anther locule. In the mutant, the anther epidermal surface was smooth, shiny, and plate-shaped compared with the three-dimensional crowded ridges and randomly formed wax crystals on the epidermal surface of the wild-type. The wild-type mature pollen had elaborate exine patterning, whereas the apv1 pollen surface was smooth. Only a few unevenly distributed Ubisch bodies were formed on the apv1 mutant, leading to a more apparent inner surface. A significant reduction in the cutin monomers was observed in the mutant. APV1 encodes a member of the P450 subfamily, CYP703A2-Zm, which contains 530 amino acids. APV1 appeared to be widely expressed in the tapetum at the vacuolation stage, and its protein signal co-localized with the endoplasmic reticulum (ER) signal. RNA-Seq data revealed that most of the genes in the fatty acid metabolism pathway were differentially expressed in the apv1 mutant. Altogether, we suggest that APV1 functions in the fatty acid hydroxylation pathway which is involved in forming sporopollenin precursors and cutin monomers that are essential for the development of pollen exine and anther cuticle in maize.

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“…Disruptions of genes in the formation and dissolution of the callose wall during the meiosis stage, including Callose synthase 5 ( CalS5 ; Dong et al ., ), CYCLIN‐DEPEDENT KINASE G1 (CDKG1; Huang et al ., ), AUXIN RESPONSE FACTOR17 ( ARF17 ; Yang et al ., ) and AtMYB103 (Zhang et al ., ), all lead to defective primexine deposition and irregular pollen exine patterns in the mutants. Disruptions of genes in the primexine formation and deposition as well as plasma membrane undulations, including DEFECTIVE EXINE FORMATION1 ( DEX1 ; Paxson‐Sowders et al ., , ), NO EXINE FORMATION1 ( NEF1 ; Ariizumi et al ., ), RUPTURED POLLEN GRAIN1 ( RPG1 ; Guan et al ., ), NO PRIMEXINE AND PLASMA MEMBRANE UNDULATION ( NPU ; Chang et al ., ), SPONGY2 ( SPG2 ; Li et al ., ), and UNEVEN PATTERN OF EXINE ( UPEX1 ; Li et al ., ) from Arabidopsis and OsDEX1 from rice (Yu et al ., ), after the tetrad formation, also result in aberrant pollen exine pattern. Obviously, the processes of callose and primexine formation are associated with pollen exine patterning.…”

Section: Introductionmentioning

confidence: 99%

Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning

et al. 2017

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Angiosperm male reproductive organs (anthers and pollen grains) have complex and interesting morphological features, but mechanisms that underlie their patterning are poorly understood. Here we report the isolation and characterization of a male sterile mutant of No Pollen 1 (NP1) in rice (Oryza sativa). The np1-4 mutant exhibited smaller anthers with a smooth cuticle surface, abnormal Ubisch bodies, and aborted pollen grains covered with irregular exine. Wild-type exine has two continuous layers; but np1-4 exine showed a discontinuous structure with large granules of varying size. Chemical analysis revealed reduction in most of the cutin monomers in np1-4 anthers, and less cuticular wax. Map-based cloning suggested that NP1 encodes a putative glucose-methanol-choline oxidoreductase; and expression analyses found NP1 preferentially expressed in the tapetal layer from stage 8 to stage 10 of anther development. Additionally, the expression of several genes involved in biosynthesis and in the transport of lipid monomers of sporopollenin and cutin was decreased in np1-4 mutant anthers. Taken together, these observations suggest that NP1 is required for anther cuticle formation, and for patterning of Ubisch bodies and the exine. We propose that products of NP1 are likely important metabolites in the development of Ubisch bodies and pollen exine, necessary for polymerization, assembly, or both.

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A Rice Ca²⁺ Binding Protein Is Required for Tapetum Function and Pollen Formation

Cited by 53 publications

References 93 publications

The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice

The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice

ABNORMAL POLLEN VACUOLATION1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize

Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning

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A Rice Ca2+ Binding Protein Is Required for Tapetum Function and Pollen Formation

Cited by 53 publications

References 93 publications

The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice

The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice

ABNORMAL POLLEN VACUOLATION1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize

Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning

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A Rice Ca²⁺ Binding Protein Is Required for Tapetum Function and Pollen Formation