The Toughest Material in the Plant Kingdom: An Update on Sporopollenin

Abstract

The extreme chemical and physical recalcitrance of sporopollenin deems this biopolymer among the most resilient organic materials on Earth. As the primary material fortifying spore and pollen cell walls, sporopollenin is touted as a critical innovation in the progression of plant life to a terrestrial setting. Although crucial for its protective role in plant reproduction, the inert nature of sporopollenin has challenged efforts to determine its composition for decades. Revised structural, chemical, and genetic experimentation efforts have produced dramatic advances in elucidating the molecular structure of this biopolymer and the mechanisms of its synthesis. Bypassing many of the challenges with material fragmentation and solubilization, insights from functional characterizations of sporopollenin biogenesis in planta, and in vitro, through a gene-targeted approach suggest a backbone of polyhydroxylated polyketide-based subunits and remarkable conservation of biochemical pathways for sporopollenin biosynthesis across the plant kingdom. Recent optimization of solid-state NMR and targeted degradation methods for sporopollenin analysis confirms polyhydroxylated α-pyrone subunits, as well as hydroxylated aliphatic units, and unique cross-linkage heterogeneity. We examine the cross-disciplinary efforts to solve the sporopollenin composition puzzle and illustrate a working model of sporopollenin's molecular structure and biosynthesis. Emerging controversies and remaining knowledge gaps are discussed, including the degree of aromaticity, cross-linkage profiles, and extent of chemical conservation of sporopollenin among land plants. The recent developments in sporopollenin research present diverse opportunities for harnessing the extraordinary properties of this abundant and stable biomaterial for sustainable microcapsule applications and synthetic material designs.

Keywords: biopolymer; exine cell wall; molecular structure; pollen; polyketide; spore; sporopollenin; α-pyrone.

Figure 1

Proposed sporopollenin metabolic pathway and simplified molecular structures of Pinus rigida and Lycopodium clavatum sporopollenin. Fatty acyl-ACP esters, synthesized de novo by the FAS complex, are reduced by MS2 to produce fatty alcohols or hydrolyzed by FATB to produce free fatty acids. After hydroxylation by CYP703A2 and CYP704B1, free fatty acids may be reduced by unknown reductases to fatty alcohols or aldehydes, forming putative hydroxylated aliphatic sporopollenin precursors. Alternatively, hydroxylation by CYP703A2 and CYP704B1 of the fatty alcohol produced by MS2 may occur. In the case of Pinus rigida, these aliphatic precursors might be acylated with phenolics by an unknown transferase. Hydroxylated or non-hydroxylated fatty acids are esterified to CoA by ACOS5 prior to several cycles of condensation by PKSs and reduction by TKPRs to form polyhydroxylated α-pyrone precursors. The precursors could be exported to the anther locule and polymerized on the surface of developing microspores by an unknown mechanism. In Pinus rigida, a simplified sporopollenin is proposed to predominantly contain hydroxylated aliphatic α-pyrone units, crosslinked at one end through an ester group and linked through a dioxane moiety to other units by a hydroxylated aliphatic chain bearing a coumaroyl moiety. In Lycopodium clavatum, the sporopollenin structure is proposed to contain a rigid macrocyclic backbone of several hydroxylated aliphatic α-pyrone units coupled through ether bonds to hydroxylated aliphatic networks linked together by glycerol.