Arabidopsis SKU5 Similar 11 and 12 play crucial roles in pollen tube integrity, growth and guidance

Abstract

SUMMARY Pollen tube integrity, growth and guidance are crucial factors in plant sexual reproduction. Members of the plant Skewed5 (SKU5) Similar (SKS) family show strong similarity to multicopper oxidases (MCOs), but they lack conserved histidines in MCO active sites. The functions of most SKS family members are unknown. Here, we show that Arabidopsis pollen‐expressed SKS11 and SKS12 play important roles in pollen tube integrity, growth and guidance. The sks11sks12 mutant exhibited significantly reduced male fertility. Most of the pollen from sks11sks12 plants burst when germinated, and the pollen tubes grew slowly and exhibited defective growth along the funiculus and micropyle. SKS11‐GFP and SKS12‐mCherry were detected at the cell wall in pollen tubes. The contents of several cell wall polysaccharides and arabinogalactans were decreased in the pollen tube cell walls of sks11sks12 plants. Staining with a reactive oxygen species (ROS)‐sensitive dye and use of the H2O2 sensor HyPer revealed that the ROS content in the pollen tubes of sks11sks12 plants was remarkably reduced. SKS11444His‐Ala, in which the last conserved histidine was mutated, could restore the mutant phenotypes of sks11sks12. Thus, SKS11/12 are required for pollen tube integrity, growth and guidance possibly by regulating the ROS level and cell wall polysaccharide deposition or remodeling in pollen tubes.

Ascorbic acid-mediated reactive oxygen species homeostasis modulates the switch from tapetal cell division to cell differentiation in Arabidopsis

“…The SKS family counts 19 members in Arabidopsis ( Sedbrook et al 2002 ). A recent study indicated that mutating the last histidine residue in the copper center of SKS11 produced a protein with enough activity to rescue the defects of the sks11 sks12 double mutant ( Duan et al 2021 ). We, therefore, suspect that some SKS proteins may have evolved new functions that do not require their copper cofactor, while others like SKS18 behave as AAOs and rely on copper stimulation.…”

“…For instance, ZmSKS13 influences kernel development through modulating ROS homeostasis ( Zhang et al 2021 ). In Arabidopsis, SKS11 and SKS12 are required for pollen tube integrity, growth, and guidance by regulating ROS levels ( Duan et al 2021 ). Pollen-expressed SKS13 affects pollination/fertilization ( Ji et al 2019 ).…”

Striking a growth–defense balance: Stress regulators that function in maize development

“…Whereas the roles of ROS in seed dormancy and germination have been extensively studied (Bailly, 2019), less attention has been given to the maintenance of ROS homeostasis during seed development. Zhang et al (2021b) (Chen et al, 2014a;Duan et al, 2022). Therefore, further investigations are needed to understand how SKS proteins modulate ROS levels in opposite manners.…”

“…SKS proteins in Arabidopsis also function in ROS homeostasis. Whereas AtSKS1 functions in ROS scavenging in a manner similar to ZmSKS13 (Chen et al, 2023), AtSKS11, AtSKS12, and AtSKS13, in contrast with ZmSKS13, promote ROS production (Chen et al, 2014a; Duan et al, 2022). Therefore, further investigations are needed to understand how SKS proteins modulate ROS levels in opposite manners.…”

Self-incompatibility requires GPI anchor remodeling by the poppy PGAP1 ortholog HLD1

“…As the ectopic "SI-like PCD" response in Arabidopsis roots 25 also requires AtPGAP1, it appears that broadly expressed GPI-APs, rather than those specifically involved in reproduction, are involved in SI. Interestingly, SKU5, which regulates directional root growth, is a member of a gene family containing pollen-expressed SKS11/12, which control pollen tube growth 54 . As well as playing a key role in cell-cell signaling during reproduction and development, GPI-APs also participate in pathogen responses 37,47,55 .…”