Three Decades of Advances in Arabinogalactan-Protein Biosynthesis

Abstract

Arabinogalactan-proteins (AGPs) are a large, complex, and highly diverse class of heavily glycosylated proteins that belong to the family of cell wall hydroxyproline-rich glycoproteins. Approximately 90% of the molecules consist of arabinogalactan polysaccharides, which are composed of arabinose and galactose as major sugars and minor sugars such as glucuronic acid, fucose, and rhamnose. About half of the AGP family members contain a glycosylphosphatidylinositol (GPI) lipid anchor, which allows for an association with the outer leaflet of the plasma membrane. The mysterious AGP family has captivated the attention of plant biologists for several decades. This diverse family of glycoproteins is widely distributed in the plant kingdom, including many algae, where they play fundamental roles in growth and development processes. The journey of AGP biosynthesis begins with the assembly of amino acids into peptide chains of proteins. An N-terminal signal peptide directs AGPs toward the endoplasmic reticulum, where proline hydroxylation occurs and a GPI anchor may be added. GPI-anchored AGPs, as well as unanchored AGPs, are then transferred to the Golgi apparatus, where extensive glycosylation occurs by the action of a variety glycosyltransferase enzymes. Following glycosylation, AGPs are transported by secretory vesicles to the cell wall or to the extracellular face of the plasma membrane (in the case of GPI-anchored AGPs). GPI-anchored proteins can be released from the plasma membrane into the cell wall by phospholipases. In this review, we present an overview of the accumulated knowledge on AGP biosynthesis over the past three decades. Particular emphasis is placed on the glycosylation of AGPs as the sugar moiety is essential to their function. Recent genetics and genomics approaches have significantly contributed to a broader knowledge of AGP biosynthesis. However, many questions remain to be elucidated in the decades ahead.

Arabinogalactan Proteins in Plant Roots – An Update on Possible Functions

“…Arabinogalactan proteins have the most extensive glycosylation of Pro/Hyp-rich glycoproteins. Their carbohydrate moiety forms 90 to 99% of their molecular mass, combining galactose and arabinose as major sugars with fucose, rhamnose, and glucuronic acid as minor sugars (Fincher et al, 1983;Ellis et al, 2010;Showalter and Basu, 2016;Silva J. et al, 2020). AGPs form a complex family (Showalter, 2001).…”

“…Their classification has been modified several times over the last decades. Most recently they have been divided into several groups according to their molecular structure: classical AGP, AG peptides, Lys-rich AGPs, chimeric AGPs including FLAs (FASCICLIN-LIKE AGPs), ENODLs (EARLY NODULIN-LIKE AGPs), XYLPs (XYLOGEN-LIKE AGPs), other chimeric AGPs, and HAEs (AGP-EXT hybrids) (Showalter, 2001;Pereira et al, 2015;Mareri et al, 2018;He et al, 2019;Silva J. et al, 2020). Classical AGPs are characterized by the presence of an N-terminal signal sequence, which targets the protein to the endoplasmic reticulum (ER) and secretory pathway, a middle PAST-rich domain (rich in Pro, Ala, Ser, and Thr), and a C-terminal sequence, which is cleaved during the establishment of the GPI (glycosylphosphatidylinositol) anchor in the ER (Schultz et al, 1998).…”

“…Lys-rich AGPs contain a Lys-rich domain between PAST domain and C-terminus, ENODLs contain plastocyanin-like domains, XYLPs contain non-specific lipid transfer protein domains, and HAEs combine modules characteristic for AGPs and EXTs. For further details of classification see recent reviews (Ma et al, 2017;Silva J. et al, 2020).…”

“…AGPs are covalently linked to pectins or hemicelluloses (Immerzeel et al, 2006;Tan et al, 2013) and their action as "pectin plasticizers" was hypothesized (Lamport et al, 2006;Corral-Martinez et al, 2019). Another putative mechanism is an enzymatic release of mobile oligosaccharides from AGP glycan side chains that may act as signaling molecules possibly recognized by plasma membrane receptors (Showalter, 2001;Van Hengel and Roberts, 2002;Zagorchev et al, 2014;Silva J. et al, 2020). In spite of studies linking activity of plant chitinases with AGPs action in developmental processes (van Hengel et al, 2001;Dos Santos et al, 2006;Zielinski et al, 2021), this mechanism needs to be proven and membrane receptors recognizing AGP-borne oligosaccharide fragments are not yet characterized.…”

Ovary Signals for Pollen Tube Guidance in Chalazogamous Mangifera indica L.

“…Arabinogalactan proteins (AGPs) have been observed along the pollen tube pathway in a number of unrelated porogamous species. AGPs are extensively glycosylated hydroxyproline (Hyp)–rich proteins ( Silva et al, 2020 ) that have been associated with the acquisition of stigmatic receptivity ( Losada and Herrero, 2012 ; Losada et al, 2014 ) and pollen tube growth in the style ( Cheung et al, 1995 ; Wu et al, 1995 ; Losada and Herrero, 2014 ). Moreover, in the ovary, where an intense pollen–pistil interaction occurs ( Herrero, 2000 , 2001 ), AGPs also appear to mediate access of the pollen tubes to the ovules at the obturator ( Losada and Herrero, 2017 ) and support pollen tube penetration to the ovule through the micropyle ( Coimbra et al, 2007 ; Lora et al, 2019 ; Losada and Herrero, 2019 ).…”