Arabidopsis ABCG28 is required for the apical accumulation of reactive oxygen species in growing pollen tubes

Abstract

Tip-focused accumulation of reactive oxygen species (ROS) is tightly associated with pollen tube growth and is thus critical for fertilization. However, it is unclear how tip-growing cells establish such specific ROS localization. Polyamines have been proposed to function in tip growth as precursors of the ROS, hydrogen peroxide. The ABC transporter AtABCG28 may regulate ROS status, as it contains multiple cysteine residues, a characteristic of proteins involved in ROS homeostasis. In this study, we found that AtABCG28 was specifically expressed in the mature pollen grains and pollen tubes. AtABCG28 was localized to secretory vesicles inside the pollen tube that moved toward and fused with the plasma membrane of the pollen tube tip. Knocking out AtABCG28 resulted in defective pollen tube growth, failure to localize polyamine and ROS to the growing pollen tube tip, and complete male sterility, whereas ectopic expression of this gene in root hair could recover ROS accumulation at the tip and improved the growth under high-pH conditions, which normally prevent ROS accumulation and tip growth. Together, these data suggest that AtABCG28 is critical for localizing polyamine and ROS at the growing tip. In addition, this function of AtABCG28 is likely to protect the pollen tube from the cytotoxicity of polyamine and contribute to the delivery of polyamine to the growing tip for incorporation into the expanding cell wall.

Oxygen radicals and cytoplasm zoning in growing lily pollen tubes

“…This pattern is quite similar to the one found in Picea pollen tubes (Maksimov et al 2018), but, as expected, apical accumulation of H 2 O 2 is larger in Lilum, with higher growth speed. Apical H 2 O 2 accumulation was as well found very short pollen tubes which agrees well with the pattern reported recently for Arabidopsis (Do et al 2019). Localization of H 2 O 2 in plastids is similar in lily and spruce, though they are much larger in Picea and contain a lot of starch .…”

Reactive Oxygen Species as Mediators of Gametophyte Development and Double Fertilization in Flowering Plants

“…Maintenance of ROS homeostasis in pollen tubes is dependent on the availability of precursors and the abundance of antioxidant scavengers. An ABC transporter, ABCG28 was shown to be required for the apical accumulation of ROS in growing pollen tubes ( Do et al., 2019 ). ABCG28 is involved in accumulation of secretory vesicles containing polyamines, precursors of ROS, at the growing tip of pollen tubes.…”

“…ABCG28 is involved in accumulation of secretory vesicles containing polyamines, precursors of ROS, at the growing tip of pollen tubes. abcg28 mutant pollen tubes have altered hydrogen peroxide distribution and fail to localize polyamine to the growing tip, resulting in defective pollen tube growth ( Do et al., 2019 ). Flavanols and anthocyanins are secondary metabolites that function as ROS scavengers in plants.…”

Exocytosis and Endocytosis: Yin-Yang Crosstalk for Sculpting a Dynamic Growing Pollen Tube Tip

“…In addition to exocytosis and endocytosis, an intricate regulatory network consisting of plant-specific Rho GTPase 1 (ROP1), actin cytoskeleton, exocyst complex proteins, phospholipids (PIs), SNARE proteins, cell wall biochemical mechanics, Ca 2+ , pH, reactive oxygen species (ROS) and so forth regulates exocytosis and endocytosis in the pollen tube tip ( Lee et al, 2008 ; Craddock et al, 2012 ; Duan et al, 2014 ; Zhou et al, 2015 ; Takeuchi and Higashiyama, 2016 ; Sekeres et al, 2017 ; Mangano et al, 2018 ; Wudick et al, 2018 ; Do et al, 2019 ; Domingos et al, 2019 ; Guo and Yang, 2020 ). Nevertheless, little is known about how these different regulatory factors are well orchestrated to function as positive and negative feedback loops in their action on exocytosis and endocytosis and thereby governing pollen tube polarization and polar growth.…”