Scientia Agricultura Sinica ›› 2019, Vol. 52 ›› Issue (8): 1295-1307.doi: 10.3864/j.issn.0578-1752.2019.08.001

Special Issue: MALE STERILITY OF CROP

• MALE STERILITY OF CROP • Previous Articles     Next Articles

The Function of the Polyketide Synthase OsPKS1 and OsPKS2 in Regulating Pollen Wall Formation in Rice

ZHOU YuLu1,LIN Hong1,ZHANG DaBing1,2,WANG CanHua1(),YU Jing1()   

  1. 1 School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240
    2 School of Agriculture, Food and Wine, University of Adelaide; Australia SA 5005
  • Received:2018-12-10 Accepted:2019-01-24 Online:2019-04-16 Published:2019-04-26
  • Contact: CanHua WANG,Jing YU E-mail:wangcanhua@sjtu.edu.cn;yujing@sjtu.edu.cn

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Abstract:

【Background】 Plant pollen is surrounded by pollen wall which acts as a natural protective barrier for male gametes and plays a pivotal role in plant reproductive development. The main component of pollen wall is sporopollenin, which is mainly composed of lipidic and phenolic substances. Therefore, the metabolism of these two substances is a key step for anther wall and pollen wall formation. PKS1/PKSA/LAP6 and PKS2/PKSB/LAP5 show conserved biochemical functions in sporopollenin biosynthesis pathways among different species. 【Objective】 The role of OsPKS1 and OsPKS2 in rice anther wall and pollen wall development was studied to provide a new understanding for the mechanism of this process. 【Method】 A gene co-expressed network, AntherNet predicted a gene OsPKS1 that might be involved in sporopollenin biosynthesis, using the CRISPR/Cas9 genome editing system to generate ospks1 and ospks1 ospks2 in Japonica subspecies 9522 background and ospks2 background, respectively. Under the same growth condition, the vegetative growth and floral organ development of the mutant plants were analyzed by comparing the phenotypes of the wild type and the mutants. I2-KI staining was utilized to analyze the pollen viability of ospks1 and ospks1 ospks2. Semi-thin section was performed to observe four cell layers and microspore development in the wild type and the mutants at different stages. Scanning electron microscope (SEM) was used to observe the fine structures of anther wall outer and inner surface as well as pollen wall surface both in the wild type and the mutants. And transmission electron microscopy (TEM) was performed to observe the fine structures of anther wall cell, Ubisch body and pollen wall of the wild type and the mutants.【Result】Four ospks1 and four ospks1 ospks2 were obtained by CRISPR/Cas9 approach, among which ospks1-3 and ospks1-4 ospks2 were homozygous mutants. Both ospks1-3 and ospks1-4 ospks2 were male sterile. ospks1-3 and ospks2 displayed abnormal pollen wall and Ubisch body, however, the detailed morphology was different between two mutants. ospks1-3 could form convex wall structure on the surface of pollen wall and the tapetal layer could be normally degraded; a large number of tiny cavities were formed in the inner structure of pollen wall and the bacula became shorter, which might cause invalid connection between tectum and nexine; the bottom structure of Ubisch bodies was decreased while the top structure was increased and Ubisch bodies were sharper than those of the wild type. By observing ospks1-4 ospks2, it was found that the cuticle was reduced and the tapetal layer could not be degraded normally. Besides, there was no obvious pollen wall structure on the surface of microspores and the microspores were degraded at stage 11; Ubisch bodies were less formed with abnormal structure at stage 9 and were detached from the anther wall at stage 11. 【Conclusion】 The function of PKS1/PKSA/LAP6 and PKS2/PKSB/LAP5 are conserved among various species and could affect the biosynthesis and accumulation of sporopollenin. However, these two genes show different function for the formation of the inner structure of pollen wall and Ubisch bodies in rice: OsPKS1 is more important for the formation of bacula and the bottom structure of Ubisch bodies; OsPKS2 is more important for the formation of tectum and the top structure of Ubisch bodies. They regulate the formation of pollen wall, anther wall and the degradation of tapetum.

Key words: Oryza sativa, OsPKS1, OsPKS2, sporopollenin, pollen wall, male sterile

Table 1

CRISPR primers and genotyping primers for OsPKS1"

引物名称
Primer name		 正向引物
Forward primer(5′-3′)		 反向引物
Reverse primer (5′-3′)
OsPKS1_Cri_T1 TAGGTCTCCCAAGGAAGAGAAGTTTTAGAGCTAGAA CGGGTCTCACTTGGCTGCTCCTGCACCAGCCGGG
OsPKS1_Cri_T2 TAGGTCTCCACTACAAGGACGGTTTTAGAGCTAGAA CGGGTCTCATAGTAGCCGCGGTGCACCAGCCGGG
OsPKS1_Cri_GT CTAGACGAGCACCCAGAGCT ACCTTGTCCGTCCCTGGTAG

Fig. 1

Target sites of the gRNA in the OsPKS1 gene and mutation site analysis A: Position of two targets in OsPKS1 gene locus, cloning of two gRNA cassettes into the pRGEB32CRISPR/Cas9 vector; B: Mutation site sequencing results of ospks1-3 and ospks1-4 ospks2; C: The protein prediction analysis of the wild type and the mutants, green boxes indicate putative conserved domain, the arrows indicate the mutation position. D: Mutation information in other alleles"

Fig. 2

The phenotypic comparison among the wild type, ospks1-3 and ospks1-4 ospks2 A: Wild-type plant (left), ospks1-3 mutant plant (middle) and ospks1-4 ospks2 mutant plant (right); B: Part of a wild-type panicle (left), an ospks1-3 panicle (middle) and an ospks1-4 ospks2 panicle (right) at seed producing stage; C-E: Wild-type flower, ospks1-3 flower and ospks1-4 ospks2 flower at stage 13 all with lemma and palea removed; F: Wild-type yellow anther and pollen grains stained with I2-KI solution at stage 13; G: ospks1-3 mutant anther and pollen grains stained with I2-KI solution at stage 13; H: ospks1-4 ospks2 mutant anther and pollen grains stained with I2-KI solution at stage 13. Pi: Pistil; St: Stamen. Bars: 10 cm (A); 5 cm (B); 2 mm (C-E), 1 mm (F-H), 200 μm in insets (F-H)"

Fig. 3

Transverse section analysis of anther development in the wild type, ospks1-3 and ospks1-4 ospks2 A-E: Wild type; F-J: ospks1-3; K-O: ospks1-4 ospks2. DMsp: Degenerated microspores; E: Epidermis; En: Endothecium; Ml: Middle layer; Msp: Microspore; T: Tapetum; Tds: Tetrads; Mp: Mature pollen; DMp: Degenerated mature pollen. Bar: 20 μm (A-O)"

Fig. 4

SEM and TEM observation for anther and pollen in the wild type and ospks1-3 A-H: SEM analysis of the surface of anthers and pollen grains in the wild type and ospks1-3 at stage 13; I-L: TEM observation of pollen wall and Ubisch body in the wild type and ospks1-3 at stage 10. A: Pollens of the wild type; B: Anther epidermis of the wild type; C: Pollen wall of the wild type; D: The inner surface of the wild type; E: Pollens of ospks1-3; F: Anther epidermis of ospks1-3; G: Pollen wall of ospks1-3; H: The inner surface of ospks1-3; I: Ultra-thin sections of pollen wall in the wild type; J: Ultra-thin sections of pollen wall in ospks1-3; K: Ultra-thin sections of Ubisch body in the wild type; L: Ultra-thin sections of Ubisch body in ospks1-3. Ex: Exine; DEx: Deformed exine; Ne: Nexine; Ub: Ubisch body; Ba: Bacula; Te: Tectum. Bars: 20 μm (A, E); 10 μm (B, F); 1 μm (C, D, G, H); 0.5 μm (I-L)"

Fig. 5

SEM observation for anther and pollen in the wild type and ospks1-4 ospks2 A: Anther epidermis of the wild type; B: The inner surface of the wild type; C: Anther epidermis of ospks1-4 ospks2; D: The inner surface of ospks1-4 ospks2. Ub: Ubisch body. Bars: 10 μm (A, C), 1 μm (B, D)"

Fig. 6

Transmission electron microscopy analysis of anthers in the wild type and ospks1- 4 ospks2 A-C: Pollen wall of the wild type from stage 9 to stage 11; D-F: Pollen wall of ospks1-4 ospks2 from stage 9 to stage 11; G-I: Ubisch body in the wild type from stage 9 to stage 11; J-L: Ubisch body in ospks1-4 ospks2 from stage 9 to stage 11. Msp: Microspore; DMsp: Degenerated microspore; AEx: Abnormal exine; Ne: Nexine; Ub: Ubisch body; T: Tapetum; Ba: Bacula; Te: Tectum; Pb: Probacula; Pe: Prim-exine. Bars: 0.5 μm"

Fig. 7

The proposed roles of OsPKS1 and OsPKS2 in anther cuticle and pollen wall development OsACOS12 catalyzes diverse fatty acids to produce fatty acyl coenzyme A which is then condensed by OsPKS1 or OsPKS2 to form different types of polyketide. Different types of polyketide involved in the formation of cutin monomers and sporopollenin precursor are required for the different structures in Ubisch body and pollen wall formation and also participate in the development of anther cuticle"

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