Molecular and Functional Roles of Tapetum Organelles: A Nursing Staff for Pollen Development

doi:10.1016/j.rsci.2025.06.003

Abstract

Abstract:

Male gametes are produced in the anthers and are essential for fertilization and seed setting. A transverse section of the anther reveals four layers: the epidermis, endothecium, middle layer, and tapetum. The tapetum, being the innermost layer, plays a critical role in supplying nutrients, enzymes, and protection to microspores. Detailed microscopic and ultrastructural analyses have revealed highly active and well-organized structures within the tapetum, referred to as tapetal organelles. Molecular studies have highlighted the significance of tapetal cell death and the nurturing role of the tapetum for microspores. However, the mechanisms by which these processes are mediated by tapetal organelles at the cellular level remain elusive. The discovery of mutants defective in tapetal organelles has enabled further investigations into their structure, morphology, and function. This review discusses the molecular and functional roles of various tapetal organelles, such as plastids (amyloplasts and elaioplasts), mitochondria, tapetosomes, endoplasmic reticulum, and lipid bodies. We provide an overview of their roles, highlight key organelles in the tapetum, and address recent challenges and potential applications of genes regulating tapetal organelles in enhancing crop fertility.

Key words: tapetum, plastid, elaioplast, amyloplast, mitochondrion, endoplasmic reticulum

Asif Ali, Sumer Zulfiqar, Asad Riaz, Maneesh Lingwan, Sun Lianping, Wu Xianjun. Molecular and Functional Roles of Tapetum Organelles: A Nursing Staff for Pollen Development[J]. Rice Science, 2025, 32(5): 617-636.

Figures/Tables 6

Fig. 1. Cytological morphology of anther’s cross section and development of pollen grain. Cytological development of the pollen grain during anther development stages is illustrated from stages 5-14, excluding stages 1-4 where tapetum is not present. In stage 5, cross section shows formation of T from SP. In stage 6, differentiation of the tapetal cells and formation of MMC, also known as pollen mother cell. In stage 7, meiosis I begins in MMC, and ML starts disappearing and ellipsoidal-shaped Dy are formed. In stage 8, MMC undergoes a further meiotic division (meiosis II), resulting in the formation of Tds. Among four haploid microspores, three free microspores degenerate and only one survives. In stage 9, callose wall is degraded by callases secreted from tapetal cells and Ubisch bodies are released from tapetal organelles and ML has disappeared and T starts degeneration. In stage 10, microspore continues to grow and becomes round and vacuolated. In stage 11, microspore goes into mitosis I and becomes sickle shaped to form a vegetative cell (large) and generative cell (small), T completely degenerated and its contents are released into anther locule for pollen exine formation. In stage 12, two sperm cells are formed from a generative cell as a result of mitosis II. In stage 13, pollen grain maturation is accomplished and anther dehiscence starts, whereas ML completely disappeared. In stage 14, mature pollen grains are released from anthers. Mature pollen grain lacks a complete MMC and callose walls at this stage. BP, Bicellular pollen; Dy, Dyad; EP, Epidermis, outermost layer of the anther; EN, Endothecium, inner layer of the anther; ML, Middle layer of the anther; MMC, Microspore mother cell; MP, Mature pollen; MSP, Megasporocyte; SP, Secondary parietal cell; T, Tapetum, innermost layer of the anther; Tds, Tetrads.

Fig. 2. Synchronous process of microsporogenesis and microgametogenesis. Flowers produce diploid (2n) microsporocytes, which undergo meiosis to produce four haploids. During early microspore development, free microspores have dense cytoplasm with small vacuoles. Each microspore goes into mitosis and bicellular pollen grains are formed. As they progress towards maturation, the cytoplasm moves to the periphery and vacuoles combine into a single large vacuole. Bicellular pollen grains contain multiple miniature vacuoles and numerous subcellular organelles. Vacuoles in tapetal cells are involved in nutrient storage and sporopollenin precursor degradation. Sporopollenin is crucial for microspore integrity and maturation and is produced by tapetal cells and protects pollen from harsh environments before germination.

Fig. 3. Essential genes and functional roles of tapetal organelles. The development of the anther is divided into 14 distinct stages based on its cytological features. The tapetum, which is an essential tissue for pollen development, appears in stage 5 and degenerates at stage 11. During stages 5-7, tapetum cells actively synthesize and process nutrition and protection required for pollen development. In stages 9-11, these precursors are delivered. Tapetum cells also secrete enzymes, hormones, amino acids, and other nutritious materials essential for pollen development. The molecularly complex deposition of lipids is regulated by tapetal organelles such as elaioplast and tapetosomes. Essential genes with functional roles are present around the surface of these organelles, which include elaioplasts, amyloplasts, lipids bodies, mitochondria, vacuoles, tapetosomes, and endoplasmic reticulum. Specific colored genes can be observed in the key.

Fig. 4. Biochemical roles of tapetal organelles and their genes in pollen development-associated processes through tricarboxylic acid cycle. The development and degradation of tapetum, the deposition of callose, the production and transport of sporopollenin, and the development of anther wax are all well-known aspects of pollen development. Sporopollenin is a major component in the formation of pollen exine, and its synthesis and transport are coordinated through various molecular and biochemical pathways. Glycolysis and pyruvate pools are reported to be transformed into tapetal cells, and C12 and C16 fatty acid molecules are ultimately processed into sporopollenin synthesis. Pyruvate pool is also converted to polysaccharides and callose walls in microspores. Acetyl-CoA is moved to the tapetal endoplasmic reticulum to form very long chain fatty acids (VLCFAs) that create anther wax. These molecules are then transported from the tapetal cells to create quercetin-7-(3)-O-glucoside and sugar nucleotides, which form the pollen coat. Tapetal cells have some reported genes, which are related to the elaioplast, amyloplast, lipid body, mitochondrion, vacuole, tapetosome, and endoplasmic reticulum. Among tapetal organelles, the endoplasmic reticulum plays its role in pollen exine formation and anther development through bZIP28, IRE1a/b, TKPR1, PKSA, PKSB, and ACOS5. Similarly, CPPR1, Tic40, GLK1, and GPT1 are associated with elaioplast and plastid development and mainly involved in tapetum cell death. ACP, Acyl carrier protein.

Table 1. Genes and proteins involved in regulating the functions of various tapetal organelles.

Name	ID	Protein		Function	Reference
Pollen wall formation
AMS	AT2G16910	bHLH transcription factor		Early tapetum development	Sorensen et al, 2003; Xu et al, 2010
DYT1	AT4G21330	bHLH transcription factor		Early tapetum development	Zhang et al, 2006
MYB80	AT5G56110	MYB transcription factor		Tapetum programmed cell death, microspore release, exine formation	Zhang et al, 2007; Xiong et al, 2016
TDF1	AT3G28470	MYB transcription factor		Early tapetum development	Zhu et al, 2008
CYP704B2	Os03g07250	Cytochrome P450		Required for anther cutin biosynthesis and pollen exine development	Li et al, 2010
ABCG15	AT3G21090	ATP binding cassette transporter		Sporopollenin transportation	Qin et al, 2013
CYP703A3	Os08g0131100	Cytochrome P450 protein		Development of anther cuticle and pollen exine	Yang et al, 2014
DPW	Os01g70025	A cytoplasmically localized BAHD acyltransferase		Pollen development	Xu et al, 2017
OsPKS2	Os07g0411300	PKS III superfamily protein		Pollen exine and Ubisch body patterning	Zhu et al, 2017
OsPKS1	Os10g34360	PKS III superfamily protein		Pollen exine formation and sporopollenin precursor biosynthetic pathway	Zou et al, 2017
Elaioplast/plastid
Tic40	AT5G16620	A putative plastid inner envelope membrane translocon		Tapetal function and microspore development	Dun et al, 2011
OsGPT1	Os08g08840	Glucose 6-phosphate/Phosphate translocator 1 protein family		Tapetum function and pollen development	Zhang et al, 2021
OsCPPR1	Os02g0110400		P-type subfamily of pentatricopeptide repeat proteins	Tapetal programmed cell death and pollen development	Zheng et al, 2022
OsGLK1	Os06g0348800		A transcription factor belonging to the MYB GARP family	Plastid differentiation and maintenance	Zheng et al, 2022
Tapetosome
RGAT1	AT1G19530		DELLA proteins	Gibberellic acid-mediated tapetum and pollen development	Qian et al, 2021
Mitochondrion
ELM1	AT5G22350		Serine/threonine protein kinase	Mitochondrial fission	Souid et al, 2006; Chen et al, 2019
COX11	LOC4330832		Nuclear-encoded mitochondrial protein	Induce plant cytoplasmic male sterility	Luo et al, 2013
DRP3A	AT4G33650		Dynamin-related protein family	Mitochondrial fission	Chen et al, 2019
DRP3B	AT2G14120		Dynamin-related protein family	Mitochondrial fission	Chen et al, 2019
Endoplasmic reticulum
SHD/ HSP90	AT4G24190		Heat shock protein 90-7	Assist in the correct folding and activation of CLV proteins, which are essential for maintaining stem cell development in the shoot apical meristem and floral meristem of Arabidopsis	Ishiguro et al, 2002; Singh et al, 2021
ACOS5	AT1G62940		Fatty acyl-CoA synthetase	Sporopollenin synthesis	de Azevedo Souza et al, 2009
ERdj3A/ TMS1	AT3G08970		Hsp40-homologous proteins, encodes a protein with DnaJ and protein disulfide isomerase, a_ERdj5_C domain	Role in thermotolerance of pollen tubes	Yang et al, 2009
TKPR1	AT4G35420		Tetraketide alpha-pyrone reductase	Sporopollenin synthesis	Grienenberger et al, 2010
PKSB	AT4G34850		Acyltransferase	Sporopollenin synthesis	Kim et al, 2010
BiP1	AT5G28540		Hsp70 protein family	Molecular chaperone Hsp70 in the endoplasmic reticulum, involved in the fusion of polar nuclei during female gametophyte development	Maruyama et al, 2014; Singh et al, 2021
PKSA	AT1G02050		Acyltransferase	Sporopollenin synthesis	Chen et al, 2011
BiP2	AT5G42020		Hsp70 family of proteins	Expressed and functional in pollen and pollen tubes	Maruyama et al, 2014; Singh et al, 2021
IRE1a	AT2G17520		Protein family of endoribonuclease	Plant development and stress responses, protecting pollen development from elevated temperature	Deng et al, 2016
IRE1b	AT5G24360		Protein family of endoribonuclease	Plant development and stress responses, protecting pollen development from elevated temperature	Deng et al, 2016
CNX1	AT5G61790		CNX/CRT protein family	Roles in vegetative growth and male gametophyte development	Vu et al, 2017
CRT1	AT1G56340		CNX/CRT protein family	Roles in vegetative growth and male gametophyte development	Vu et al, 2017; Singh et al, 2021
bZIP28	AT3G10800		Basic leucine zipper family of transcription factors	Regulator of reproductive development and fertility genes in plants and participates in unfolded protein response in response to heat stress	Zhang et al, 2017
Vacuole
APV1	GRMZM5G830329		A member of P450 subfamily	Role in development of pollen exine and anther cuticle	Somaratne et al, 2017
Lipid body
nef1	AT5g13390		A novel plant protein of 1123 amino acids	Role in pollen development and lipid accumulation within the tapetum	Ariizumi et al, 2004
ATG7	Os01g0614900		Autophagy-related protein	Involved in metabolic regulation and nutrient supply in anthers, critical for post-meiotic anther development and pollen maturation	Kurusu et al, 2014
OsLTP47	Os02g51590		Non-specific lipid transfer protein	Function in a lipid transfer relay essential for pollen wall development	Chen et al, 2022
Amyloplast
FLO6	Os06g46350		A CBM48 domain-containing protein	Involved in compound granule formation and starch synthesis in rice endosperm	Peng et al, 2014
OsCER1	AK066386		Ceramide synthase family	Biosynthesis of very long-chain alkanes and tapetum degeneration	Ni et al, 2018
Autophagosome
SlMYB72	Solyc07g055000		MYB transcription factor	Tapetum degradation and pollen development	Wu et al, 2023

Table 1. Genes and proteins involved in regulating the functions of various tapetal organelles.

Name	ID	Protein		Function	Reference
Pollen wall formation
AMS	AT2G16910	bHLH transcription factor		Early tapetum development	Sorensen et al, 2003; Xu et al, 2010
DYT1	AT4G21330	bHLH transcription factor		Early tapetum development	Zhang et al, 2006
MYB80	AT5G56110	MYB transcription factor		Tapetum programmed cell death, microspore release, exine formation	Zhang et al, 2007; Xiong et al, 2016
TDF1	AT3G28470	MYB transcription factor		Early tapetum development	Zhu et al, 2008
CYP704B2	Os03g07250	Cytochrome P450		Required for anther cutin biosynthesis and pollen exine development	Li et al, 2010
ABCG15	AT3G21090	ATP binding cassette transporter		Sporopollenin transportation	Qin et al, 2013
CYP703A3	Os08g0131100	Cytochrome P450 protein		Development of anther cuticle and pollen exine	Yang et al, 2014
DPW	Os01g70025	A cytoplasmically localized BAHD acyltransferase		Pollen development	Xu et al, 2017
OsPKS2	Os07g0411300	PKS III superfamily protein		Pollen exine and Ubisch body patterning	Zhu et al, 2017
OsPKS1	Os10g34360	PKS III superfamily protein		Pollen exine formation and sporopollenin precursor biosynthetic pathway	Zou et al, 2017
Elaioplast/plastid
Tic40	AT5G16620	A putative plastid inner envelope membrane translocon		Tapetal function and microspore development	Dun et al, 2011
OsGPT1	Os08g08840	Glucose 6-phosphate/Phosphate translocator 1 protein family		Tapetum function and pollen development	Zhang et al, 2021
OsCPPR1	Os02g0110400		P-type subfamily of pentatricopeptide repeat proteins	Tapetal programmed cell death and pollen development	Zheng et al, 2022
OsGLK1	Os06g0348800		A transcription factor belonging to the MYB GARP family	Plastid differentiation and maintenance	Zheng et al, 2022
Tapetosome
RGAT1	AT1G19530		DELLA proteins	Gibberellic acid-mediated tapetum and pollen development	Qian et al, 2021
Mitochondrion
ELM1	AT5G22350		Serine/threonine protein kinase	Mitochondrial fission	Souid et al, 2006; Chen et al, 2019
COX11	LOC4330832		Nuclear-encoded mitochondrial protein	Induce plant cytoplasmic male sterility	Luo et al, 2013
DRP3A	AT4G33650		Dynamin-related protein family	Mitochondrial fission	Chen et al, 2019
DRP3B	AT2G14120		Dynamin-related protein family	Mitochondrial fission	Chen et al, 2019
Endoplasmic reticulum
SHD/ HSP90	AT4G24190		Heat shock protein 90-7	Assist in the correct folding and activation of CLV proteins, which are essential for maintaining stem cell development in the shoot apical meristem and floral meristem of Arabidopsis	Ishiguro et al, 2002; Singh et al, 2021
ACOS5	AT1G62940		Fatty acyl-CoA synthetase	Sporopollenin synthesis	de Azevedo Souza et al, 2009
ERdj3A/ TMS1	AT3G08970		Hsp40-homologous proteins, encodes a protein with DnaJ and protein disulfide isomerase, a_ERdj5_C domain	Role in thermotolerance of pollen tubes	Yang et al, 2009
TKPR1	AT4G35420		Tetraketide alpha-pyrone reductase	Sporopollenin synthesis	Grienenberger et al, 2010
PKSB	AT4G34850		Acyltransferase	Sporopollenin synthesis	Kim et al, 2010
BiP1	AT5G28540		Hsp70 protein family	Molecular chaperone Hsp70 in the endoplasmic reticulum, involved in the fusion of polar nuclei during female gametophyte development	Maruyama et al, 2014; Singh et al, 2021
PKSA	AT1G02050		Acyltransferase	Sporopollenin synthesis	Chen et al, 2011
BiP2	AT5G42020		Hsp70 family of proteins	Expressed and functional in pollen and pollen tubes	Maruyama et al, 2014; Singh et al, 2021
IRE1a	AT2G17520		Protein family of endoribonuclease	Plant development and stress responses, protecting pollen development from elevated temperature	Deng et al, 2016
IRE1b	AT5G24360		Protein family of endoribonuclease	Plant development and stress responses, protecting pollen development from elevated temperature	Deng et al, 2016
CNX1	AT5G61790		CNX/CRT protein family	Roles in vegetative growth and male gametophyte development	Vu et al, 2017
CRT1	AT1G56340		CNX/CRT protein family	Roles in vegetative growth and male gametophyte development	Vu et al, 2017; Singh et al, 2021
bZIP28	AT3G10800		Basic leucine zipper family of transcription factors	Regulator of reproductive development and fertility genes in plants and participates in unfolded protein response in response to heat stress	Zhang et al, 2017
Vacuole
APV1	GRMZM5G830329		A member of P450 subfamily	Role in development of pollen exine and anther cuticle	Somaratne et al, 2017
Lipid body
nef1	AT5g13390		A novel plant protein of 1123 amino acids	Role in pollen development and lipid accumulation within the tapetum	Ariizumi et al, 2004
ATG7	Os01g0614900		Autophagy-related protein	Involved in metabolic regulation and nutrient supply in anthers, critical for post-meiotic anther development and pollen maturation	Kurusu et al, 2014
OsLTP47	Os02g51590		Non-specific lipid transfer protein	Function in a lipid transfer relay essential for pollen wall development	Chen et al, 2022
Amyloplast
FLO6	Os06g46350		A CBM48 domain-containing protein	Involved in compound granule formation and starch synthesis in rice endosperm	Peng et al, 2014
OsCER1	AK066386		Ceramide synthase family	Biosynthesis of very long-chain alkanes and tapetum degeneration	Ni et al, 2018
Autophagosome
SlMYB72	Solyc07g055000		MYB transcription factor	Tapetum degradation and pollen development	Wu et al, 2023

Fig. 5. Tapetum and its organelle-associated genes: A gateway to pollen fertility and applications in crop breeding. Schematic overview of tapetum organelles contributing to pollen wall formation, nutrient secretion, and sporopollenin synthesis, enabling advances in pollen fertility, male sterility, and crop breeding program. ER, Endoplasmic reticulum; PCD, Programmed cell death; ROS, Reactive oxygen species; SPT, Seed production technology.

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