Secretory COPII Protein SEC31B Is Required for Pollen Wall Development

Abstract

The pollen wall protects pollen grains from abiotic and biotic stresses. During pollen wall development, tapetal cells play a vital role by secreting proteins, signals, and pollen wall material to ensure microspore development. But the regulatory mechanism underlying the secretory pathway of the tapetum is largely unknown. Here, we characterize the essential role of the Arabidopsis (Arabidopsis thaliana) COPII protein SECRETORY31B (SEC31B) in pollen wall development and the secretory activity of tapetal cells. The sporophyte-controlled atsec31b mutant exhibits severe pollen and seed abortion. Transmission electron microscopy observation indicates that pollen exine formation in the atsec31b mutant is disrupted significantly. AtSEC31B is a functional COPII protein revealed by endoplasmic reticulum (ER) exit site localization, interaction with AtSEC13A, and retarded ER-Golgi protein trafficking in the atsec31b mutant. A genetic tapetum-specific rescue assay indicates that AtSEC31B functions primarily in the tapetum. Moreover, deletion of AtSEC31B interrupted the formation of the ER-derived tapetosome and altered the location of the ATP-BINDING CASSETTE TRANSPORTER9 protein in the tapetum. Therefore, this work demonstrates that AtSEC31B plays a vital role in pollen wall development by regulating the secretory pathway of the tapetal cells.

The Arabidopsis COPII components, AtSEC23A and AtSEC23D, are essential for pollen wall development and exine patterning

“…Despite the low pollen germination rate, the atsec23a mutant was normally fertile, which may be due to the sufficient amount of functional pollen grains required for fertilization. Mutations in AtSEC24A , AtSEC24B , and AtSEC31B , other members of COPII, have also been shown to cause compromised pollen germination ( Conger et al , 2011 ; Tanaka et al , 2013 ; Zhao et al , 2016 ). During pollen germination, the growing pollen tube is encased only by the intine ( Chebli et al , 2012 ).…”

“…Pollen wall integrity must be maintained to ensure normal pollen development. Mutations in genes that affect pollen wall integrity, such as MALE STERILITY1 ( MS1 ), MS2 , CALLOSE SYNTHASE5 ( CALS5 ), CYTOCHROME P450 ( CYP703A2 ), RUPTURED POLLEN GRAIN1 ( RPG1 ), DEFECTIVE IN EXINE PATTERNING1 ( DEX1 ), NO EXINE FORMATION1 ( NEF1 ), TRANSIENT DEFECTIVE EXINE ( TDE1 ), ATP-binding cassette transporter G26 ( ABCG26 ), and the COPII component AtSEC31B , have resulted in collapsed pollen grains with degenerated cytoplasm ( Aarts et al , 1997 ; Paxson-Sowders et al , 1997 ; Wilson et al , 2001 ; Ariizumi et al , 2004 , 2008 ; Dong et al , 2005 ; Morant et al , 2007 ; Guan et al , 2008 ; Choi et al , 2011 ; Paxson-Sowders et al , 2001 ; Zhao et al , 2016 ). Interestingly, the mutants dex1 , nef1 , tde1 , abcg26 , and atsec31b have accumulated sporopollenin-like aggregations on the middle layer similar to the atsec23ad mutant.…”

“…The specific interaction between AtSAR1 and AtSEC23A is required for their function in ER export of proteins ( Zeng et al , 2015 ). More recently, AtSEC31B was reported to be required for pollen wall development, probably by regulating the early secretory pathway of tapetal cells ( Zhao et al , 2016 ).…”

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

“…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.…”

The Arabidopsis GPR1 Gene Negatively Affects Pollen Germination, Pollen Tube Growth, and Gametophyte Senescence

“…Main components of pollen exine are fatty acid derivatives and phenolics [ 27 , 28 , 29 ]. A growing number of genes have been identified that are important for pollen exine formation, such as MALE STERILITY2 [ 30 ], CYP703A2 and CYP704B2 [ 31 , 32 ]; RUPTURED POLLEN GRAIN1 ( RPG1 ), which are involved in fatty acid metabolism [ 33 ]; At5g62080 and At5g07230, genes encoding type III lipid transfer proteins [ 34 ]; AtbZIP34 , which encodes a bZIP-family transcription factor [ 35 ]; AtSEC31B , which encodes a secretory COPII protein [ 36 ]. Mutations of these genes usually cause severe pollen exine deposition or patterning defects, and lead to male sterility.…”