Arabidopsis ADP‐RIBOSYLATION FACTOR‐A1s mediate tapetum‐controlled pollen development

SUMMARY Propagation of angiosperms mostly relies on sexual reproduction, in which gametophytic development is a pre‐requisite. Male gametophytic development requires both gametophytic and sporophytic factors, most importantly early secretion and late programmed cell death of the tapetum. In addition to transcriptional factors, proteins at endomembrane compartments, such as receptor‐like kinases and vacuolar proteases, control tapetal function. The cellular machinery that regulates their distribution is beginning to be revealed. We report here that ADP‐RIBOSYLATION FACTOR‐A1s (ArfA1s) are critical for tapetum‐controlled pollen development. All six ArfA1s in the Arabidopsis genome are expressed during anther development, among which ArfA1b is specific to the tapetum and developing microspores. Although the ArfA1b loss‐of‐function mutant showed no pollen defects, probably due to redundancy, interference with ArfA1s by a dominant negative approach in the tapetum resulted in tapetal dysfunction and pollen abortion. We further showed that all six ArfA1s are associated with the Golgi and the trans‐Golgi network/early endosome, suggesting that they have roles in regulating post‐Golgi trafficking to the plasma membrane or to vacuoles. Indeed, we demonstrated that the expression of ArfA1bDN interfered with the targeting of proteins critical for tapetal development. The results presented here demonstrate a key role of ArfA1s in tapetum‐controlled pollen development by mediating protein targeting through post‐Golgi trafficking routes. Significance Statement By using the expression of dominant negative ADP‐RIBOSYLATION FACTOR‐A1s (ArfA1s) driven by tapetum‐specific promoters, this study demonstrates that Arabidopsis ArfA1s redundantly mediate tapetal control of pollen development. The roles of ArfA1s in the tapetum are played out via their activity both in post‐Golgi secretion and vacuolar trafficking.