The cell biology of secondary cell wall biosynthesis

Abstract

Background: Secondary cell walls (SCWs) form the architecture of terrestrial plant biomass. They reinforce tracheary elements and strengthen fibres to permit upright growth and the formation of forest canopies. The cells that synthesize a strong, thick SCW around their protoplast must undergo a dramatic commitment to cellulose, hemicellulose and lignin production.

Scope: This review puts SCW biosynthesis in a cellular context, with the aim of integrating molecular biology and biochemistry with plant cell biology. While SCWs are deposited in diverse tissue and cellular contexts including in sclerenchyma (fibres and sclereids), phloem (fibres) and xylem (tracheids, fibres and vessels), the focus of this review reflects the fact that protoxylem tracheary elements have proven to be the most amenable experimental system in which to study the cell biology of SCWs.

Conclusions: SCW biosynthesis requires the co-ordination of plasma membrane cellulose synthases, hemicellulose production in the Golgi and lignin polymer deposition in the apoplast. At the plasma membrane where the SCW is deposited under the guidance of cortical microtubules, there is a high density of SCW cellulose synthase complexes producing cellulose microfibrils consisting of 18-24 glucan chains. These microfibrils are extruded into a cell wall matrix rich in SCW-specific hemicelluloses, typically xylan and mannan. The biosynthesis of eudicot SCW glucuronoxylan is taken as an example to illustrate the emerging importance of protein-protein complexes in the Golgi. From the trans-Golgi, trafficking of vesicles carrying hemicelluloses, cellulose synthases and oxidative enzymes is crucial for exocytosis of SCW components at the microtubule-rich cell membrane domains, producing characteristic SCW patterns. The final step of SCW biosynthesis is lignification, with monolignols secreted by the lignifying cell and, in some cases, by neighbouring cells as well. Oxidative enzymes such as laccases and peroxidases, embedded in the polysaccharide cell wall matrix, determine where lignin is deposited.

Fig. 1.

SCWs in primary and secondary stem growth. Illustrative examples of SCWs in water-conducting cells (vessels, tracheids) and supportive fibres. (A and B) SCWs in primary growth. (A) SCWs in monocot primary growth exemplified in a cross-section of a grass stem internode where vascular bundles with large metaxylem vessels are encased in SCW-rich sclerenchyma (e.g. Brachypodium). (B) SCWs in eudicot primary growth illustrated in a stem cross-section prior to onset of secondary thickening (e.g. Brassica). SCWs are found in the vascular vessels and fibres, which are continuous with the thick interfascicular fibres. (C and D) SCWs in secondary growth, marked by the presence of the vascular cambium. (C) Gymnosperm secondary growth showing thick SCWs in the water-conducting and supportive tracheids of the secondary xylem (e.g. Pinus). (D) Angiosperm secondary growth showing SCWs in the water-conducting vessels and the supportive fibres (e.g. Populus).

Fig. 2.

The onset and completion of secondary cell wall (SCW) synthesis involves changes in many cellular processes. The transition from primary cell wall (PCW) to SCW deposition encompasses reorganization of microtubules, an exchange of primary cellulose synthases (CESAs) for specialized secondary CESAs and a shift in Golgi production from primary wall pectins and hemicelluloses (e.g. xyloglucan and arabinoxylans) to secondary wall hemicelluloses (e.g. xylans and mannans). Lignification occurs later in SCW production, though the lignin monomers (monolignols) and oxidative enzymes (e.g. laccases and peroxidases) required for their polymerization may be synthesized and secreted earlier. Cells that are dead at maturity undergo programmed cell death, after which lignification may continue using monolignols produced by neighbouring parenchyma.

Fig. 3.

Cellular changes accompanying SCW biosynthesis. (A) Part of a developing protoxylem tracheary element prior to SCW deposition (left) is seen in cross-section (right). Primary CESA complexes (CSCs) (red) in the plasma membrane (PM) produce cellulose for the primary cell wall (PCW). Accompanied secretory vesicles (turquoise) deliver hemicelluloses, pectins and glycoproteins to the wall by fusing with the PM. Microtubules (MTs) are widely dispersed and run roughly perpendicular to the long axis of the cell. Also shown are the endoplasmic reticulum (ER), a multivesicular body (MVB) and the vacuole. (B) Production of SCWs in protoxylem results in a helical SCW (left). A cross-section of a single SCW thickening (right) shows that microtubules have become bundled and line the PM at the region of SCW formation. A dense population of secondary wall CSCs (green) are restricted to the SCW domain. Vesicles traffic CSCs and deliver hemicelluloses (e.g. xylan and mannan) and glycoproteins (e.g. laccases) to the SCW.

Fig. 4.

Cross-section of part of a SCW-producing Golgi cisterna. The Golgi contains resident proteins (e.g. xylan biosynthetic complexes, CESA-like mannan synthase and substrate transporters) and cargo (hemicelluloses such as xylan and mannan, glycoproteins such as laccases, and CESAs), which are modified or produced in the Golgi and secreted to the SCW.