ArticleLife & Medical SciencesThe functional analysis of OsTDF1 reveals a conserved genetic pathway for tapetal development between rice and Arabidopsis
Introduction
In flowing plants, the anther is a bilaterally symmetrical structure with four lobes yielding mature pollen grains [1]. In each lobe, the cells divide and differentiate to form four distinct somatic cell layers. During meiosis, tapetal cells undergo dramatic morphological changes to acquire nutritive functions for microspores, which develop into polar secretory cells with a binuclear and condensed cytoplasm [2]. Tapetal cells play an important role in pollen development by contributing to microspore release and nutrition and sporopollenin synthesis and deposition 3., 4., 5., 6., 7.. During the late stages of anther development, tapetal cells undergo programmed cell death (PCD) to release numerous elaioplasts and cytoplasmic lipid bodies into the cavities of the exine surface as a pollen grain coating [8].
In Arabidopsis, several transcription factors (TFs) that are essential for tapetum and pollen development have been reported. DYSFUNCTIONAL TAPETUM1 (DYT1) and ABORTED MICROSPORES (AMS) are bHLH family members 9., 10.. DEFECTIVE in TAPETAL DEVELOPMENT and FUNCTION1 (TDF1) and MS188/MYB80 are two R2R3 MYB transcription factors 11., 12., 13., 14.. MALE STERILITY1 (MS1) encodes a PHD-finger family protein 15., 16.. These regulators form a genetic pathway (DYT1–TDF1–AMS–MS188–MS1) based on the analysis of double mutants and gene expression [17]. In this pathway, DYT1, TDF1 and AMS are sequentially activated to regulate early tapetum development, whereas AtMYB103 and MS1 are subsequently activated for late tapetum development and pollen wall formation. DYT1 directly regulates TDF1 for tapetum development and pollen wall formation [18].
In rice, several TFs that are essential for tapetal development and function have been identified. UNDEVELOPED TAPETUM1 (UDT1), a homolog of DYT1, plays an important role in maintaining tapetum development from early meiosis [19]. TAPETUM DEGENERATION RETARDATION (TDR), a homolog of AMS, interacts with other bHLH members, ETERNAL TAPETUM1/DELAYED TAPETUM DEGENERATION (EAT1/DTD) and bHLH142, to regulate tapetum development and degeneration via the modulation of protease expression 20., 21., 22., 23.. Sequence analysis and transgenic models have shown that Os04g39470 (OsMYB103/OsMYB80) is an ortholog of MS188 that is essential for tapetum development and pollen wall formation in rice [24]. PERSISTENT TAPETAL CELL1 (PTC1) regulates programmed tapetal development and pollen wall formation, thereby fulfilling a similar function as its homolog, MS1 [25]. In the present study, we identified the ortholog of TDF1 in rice and investigated the function of this protein in tapetum development and pollen formation. Based on these and previous results, we propose a genetic pathway for tapetum development and function in rice.
Section snippets
Mutant materials and growth conditions
The ostdf1 mutant was obtained from RISD DB (http://cbi.khu.ac.kr/RISD_DB.html). Seeds from ostdf1 and wild-type rice (Oryza sativa) were germinated for 1 week at 27 °C under continuous light and were subsequently transplanted to soil at Shanghai Normal University, located in Shanghai, China. The Arabidopsis wild-type (ecotype Ler) and tdf1 plants were grown on vermiculite at 22 °C under a 16-h light/8-h dark photoperiod.
Characterization of the mutant phenotype
The plants or flowers were photographed using a Nikon D7000 digital camera
LOC_Os03g18480 (OsTDF1) is the rice ortholog of Arabidopsis TDF1
When the amino acid sequence of Arabidopsis TDF1 was used as the query in a TBLASTN search of the rice genome, this gene showed the highest sequence similarity with the LOC_Os03g18480 in rice (O. sativa) (http://www.ncbi.nlm.nih.gov/). Conversely, when LOC_Os03g18480 was used in a TBLASTN search of the Arabidopsis genome, this gene also showed the highest sequence similarity with Arabidopsis TDF1. Therefore, LOC_Os03g18480 was designated as OsTDF1 in the present study. OsTDF1 encodes a protein
OsTDF1 is essential for tapetum development in rice
TDF1 is an essential regulator for early tapetum development in Arabidopsis [11]. Based on the sequence similarity between Arabidopsis and rice, LOC_Os03g18480 (OsTDF1) was identified as an ortholog of TDF1. Both RT-PCR analysis and in situ hybridization support the function of this protein in tapetum development in rice (Fig. 1c-e). The ostdf1 mutant exhibits abnormally vacuolated and enlarged tapetal cells that occupy the locule space during anther development (Fig. 3u-y), suggesting that
Conflict of interest
The authors declare that they have no conflict of interest.
Acknowledgments
This work was supported by the grants from the Ministry of Science and Technology of China (2013CB945100), the National Natural Science Foundation of China (31100227).
References (32)
- et al.
Regulation of β-1,3 glucanase activity in developing anthers of Lilium
Dev Biol
(1973) - et al.
A novel rice bHLH transcription factor, DTD, acts coordinately with TDR in controlling tapetum function and pollen development
Mol Plant
(2013) - et al.
Anther development: basic principles and practical applications
Plant Cell
(1993) - et al.
The tapetum: its form, function, and possible phylogeny in Embryophyta
Plant Syst Evol
(1985) - et al.
Induction of male sterility in plants by a chimeric ribonuclease gene
Nature
(1990) - et al.
Studies on heteromorphic selfincompatibility systems: the cytochemistry and ultrastructure of the tapetum of Primula obconica
J Cell Sci
(1981) The remarkable biology of pollen
Plant Cell
(1992)- et al.
Biogenesis and function of the lipidic structures of pollen grains
Sex Plant Reprod
(1998) - et al.
Programmed cell death in plant reproduction
Plant Mol Biol
(2000) - et al.
Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor
Development
(2006)
The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor
Plant J
Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis
Plant J
Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis
Plant J
AtMYB103 is a crucial regulator of several pathways affecting Arabidopsis anther development
Sci China Life Sci
The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana
Plant Cell
Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development
Plant Cell
Cited by (61)
Reproductive tissue-specific translatome of a rice thermo-sensitive genic male sterile line
2022, Journal of Genetics and GenomicsCitation Excerpt :GO enrichment analysis showed that most DE-lncRNA target genes were associated with tapetum and pollen development-specific genes (Fig. 4D; Table S11). OsC4, predicted target of the up-regulated lncRNA TCONS_00017823 (Fig. 4E) and TDF1, predicted target of up-regulated lncRNA TCONS_00042304 (Fig. 4F) are involved in lipid metabolism and tapetum PCD (Cai et al., 2015) and were down-regulated in Zhu1S in the present study (Figs. 1D and 3F). Moreover, the two genes also show decreased TE in Zhu1S (Fig. 3C) These results indicated that ribosome-associated lncRNAs might be involved in gametophyte development via mediating the expression of tapetum and pollen-related genes and thus affect fertility in TGMS rice.
Genome-wide analyses on transcription factors and their potential microRNA regulators involved in maize male fertility
2021, Crop JournalCitation Excerpt :Specifically, the Arabidopsis core regulatory pathway is composed of five TF genes including DYSFUNCTIONAL TAPETUM 1 (DYT1) [16], TAPETAL DEVELOPMENT AND FUNCTION 1 (TDF1) [17], ABORTED MICROSPORE (AtAMS) [18], AtMYB103 [19], and AtMS1 [20]. In rice, the orthologous genes of the five Arabidodpsis TF genes have been cloned, including UNDEVELOPED TAPETUM 1 (UDT1) [21], OsTDF [22], TAPETUM DEGENERATION RETARDATION (TDR) [23], OsMYB80 [24], and PERSISTANT TAPETAL CELL 1 (PTC1) [25], and the loss-of-function mutant of each gene exhibited male sterility. Furthermore, the transcriptional regulatory pathway reported in Arabidodpsis for tapetum development is relatively conserved in rice [15], and may be also conserved in maize [4].
Revealing the role of CCoAOMT1: fine-tuning bHLH transcription factors for optimal anther development
2024, Science China Life Sciences