Polygalacturonase45 cleaves pectin and links cell proliferation and morphogenesis to leaf curvature in Arabidopsis thaliana

Abstract

Regulating plant architecture is a major goal in current breeding programs. Previous studies have increased our understanding of the genetic regulation of plant architecture, but it is also essential to understand how organ morphology is controlled at the cellular level. In the cell wall, pectin modification and degradation are required for organ morphogenesis, and these processes involve a series of pectin-modifying enzymes. Polygalacturonases (PGs) are a major group of pectin-hydrolyzing enzymes that cleave pectin backbones and release oligogalacturonides (OGs). PG genes function in cell expansion and separation, and contribute to organ expansion, separation and dehiscence in plants. However, whether and how they influence other cellular processes and organ morphogenesis are poorly understood. Here, we characterized the functions of Arabidopsis PG45 (PG45) in organ morphogenesis using genetic, developmental, cell biological and biochemical analyses. A heterologously expressed portion of PG45 cleaves pectic homogalacturonan in vitro, indicating that PG45 is a bona fide PG. PG45 functions in leaf and flower structure, branch formation and organ growth. Undulation in pg45 knockout and PG45 overexpression leaves is accompanied by impaired adaxial-abaxial polarity, and loss of PG45 shortens the duration of cell proliferation in the adaxial epidermis of developing leaves. Abnormal leaf curvature is coupled with altered pectin metabolism and autogenous OG profiles in pg45 knockout and PG45 overexpression leaves. Together, these results highlight a previously underappreciated function for PGs in determining tissue polarity and regulating cell proliferation, and imply the existence of OG-based signaling pathways that modulate plant development.

Cloning and Functional Identification of SlPG49 in Solanum lycopersicum

“…Previous studies have demonstrated that a PG protein in Brassica campestris, BcMF23, was a secreted protein and exhibited extracellular localization by subcellular localization of onion epidermis transient expression [50]. In transgenic Arabidopsis, ATPGX3 and AtPG45 were located in the cell wall [51,52]. The present transient expression result in the onion epidermis confirmed that SlPG49 was a secreted protein and may play a great role in the cell wall or extracellular matrix (Figure 3), similar to PGs in A. thaliana.…”

“…The present transient expression result in the onion epidermis confirmed that SlPG49 was a secreted protein and may play a great role in the cell wall or extracellular matrix (Figure 3), similar to PGs in A. thaliana. To date, only nine PG genes have been identified in A. thaliana, with five that have been proven to show PG activity in vitro [51,[53][54][55]. However, there is no report of in vitro activity of PGs in tomatoes.…”

Thidiazuron Promotes Leaf Abscission by Regulating the Crosstalk Complexities between Ethylene, Auxin, and Cytokinin in Cotton

“…Pectinaseterase hydrolyzes the methyl ester in the pectin and promotes the production of pectic acid, which may be the substrate of PG. PG hydrolyzes the pectin substance in the intercellular layer during cell separation [ 13 , 14 ]. The effects of specific functional genes on organ shedding may be common to different species, but the signals that trigger their expression may be different [ 9 ].…”

The Root Hair Development of Pectin Polygalacturonase PGX2 Activation Tagging Line in Response to Phosphate Deficiency

“…Several Arabidopsis PG genes from the large polygalacturonase gene family have been recently reported to function in hypocotyl elongation, leaf and flower morphogenesis, pollen and pollen tube development, and stem growth ( Ogawa et al, 2009 ; Xiao et al, 2014 , 2017 ; Rui et al, 2017 ; Hocq et al, 2020 ; Yang et al, 2021 ). Importantly, we previously reported that the polygalacturonase gene, PGX2 , affects primary root length ( Xiao et al, 2017 ).…”

“…In addition, ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 ( ADPG1 ) and ADPG2 regulate floral organ abscission and anther dehiscence ( Ogawa et al, 2009 ). Recently, another polygalacturonase, PG45 functions in leaf curvature ( Yang et al, 2021 ). These characterized polygalacturonase genes are from different clades of phylogenetic tree ( Xiao et al, 2014 ) and play important functions in multiple different organs during plant growth and development.…”