The polyketide pathway in sporopollenin biosynthesis is specific to land plants (Embryophyta)

Background and AimsSporopollenin (SP) is a complex biopolymer in the outer wall of spores and pollen and provides protection from environmental stresses. Its extraordinary chemical resistance, especially to acetolysis, was widely used to identify SP in biological specimens. This broad definition of SP led to claims for its widespread occurrence among diverse embryophyte and non-embryophyte taxa. We previously proposed a biochemical definition that can be used to distinguish genuine SP from other chemically resistant cell wall materials. The definition was centred on ASCL (Anther-Specific Chalcone synthase-Like), an embryophyte-specific enzyme of the polyketide pathway that provides precursors for SP biosynthesis. Herein, we examine the evolution and distribution of all five enzymes (CYP703A, CYP704B, ACOS, ASCL and TKPR) of the polyketide pathway and propose a new, more comprehensive definition of SP. MethodsWe performed BLASTp searches, phylogenetic tree construction, protein modeling and sequence analysis to determine the presence or absence of ACOS and TKPR in embryophytes and streptophytic algae. Key ResultsWe found evidence that all five enzymes of the polyketide pathway evolved from ancestral enzymes of primary metabolism and ACOS, ASCL and TKPR were co-selected during evolution. The dosage of all five genes has been subjected to strict evolutionary control and, in some taxa, synteny has provided a selective advantage. All five enzymes are present in embryophytes but absent in green algae, indicating that the polyketide pathway and therefore SP is embryophyte-specific. ConclusionsThe addition of the polyketide pathway in the definition of genuine SP will allow separation of SP from algaenans and other chemically resistant SP-like algal spore wall substances. This study further signifies SP as an evolutionary innovation unique to the embryophyte lineage and encourages research on possible evolutionary relationship between algal spore wall SP-like materials and embryophyte SP.