Expression of the KNOTTED HOMEOBOX Genes in the Cactaceae Cambial Zone Suggests Their Involvement in Wood Development

Abstract

The vascular cambium is a lateral meristem that produces secondary xylem (i.e., wood) and phloem. Different Cactaceae species develop different types of secondary xylem; however, little is known about the mechanisms underlying wood formation in the Cactaceae. The KNOTTED HOMEOBOX (KNOX) gene family encodes transcription factors that regulate plant development. The role of class I KNOX genes in the regulation of the shoot apical meristem, inflorescence architecture, and secondary growth is established in a few model species, while the functions of class II KNOX genes are less well understood, although the Arabidopsis thaliana class II KNOX protein KNAT7 is known to regulate secondary cell wall biosynthesis. To explore the involvement of the KNOX genes in the enormous variability of wood in Cactaceae, we identified orthologous genes expressed in species with fibrous (Pereskia lychnidiflora and Pilosocereus alensis), non-fibrous (Ariocarpus retusus), and dimorphic (Ferocactus pilosus) wood. Both class I and class II KNOX genes were expressed in the cactus cambial zone, including one or two class I paralogs of KNAT1, as well as one or two class II paralogs of KNAT3-KNAT4-KNAT5. While the KNOX gene SHOOTMERISTEMLESS (STM) and its ortholog ARK1 are expressed during secondary growth in the Arabidopsis and Populus stem, respectively, we did not find STM orthologs in the Cactaceae cambial zone, which suggests possible differences in the vascular cambium genetic regulatory network in these species. Importantly, while two class II KNOX paralogs from the KNAT7 clade were expressed in the cambial zone of A. retusus and F. pilosus, we did not detect KNAT7 ortholog expression in the cambial zone of P. lychnidiflora. Differences in the transcriptional repressor activity of secondary cell wall biosynthesis by the KNAT7 orthologs could therefore explain the differences in wood development in the cactus species.

Structural Characterization of Lignin in Four Cacti Wood: Implications of Lignification in the Growth Form and Succulence

“…It has been hypothesized that the evolution of succulent growth form was greatly influenced by internal anatomical novelties in the stem, particularly those of the wood (Altesor et al, 1994 ; Carlquist, 2001 ; Mauseth, 2006 ). Such features involve an increased capacity of wood for water retention (Mauseth, 2006 ), very specialized tracheary elements with a limited secondary cell wall extension (Figure 1 ; Carlquist, 2001 ; Terrazas and Mauseth, 2002 ; Grego-Valencia et al, 2015 ; Reyes-Rivera et al, 2017 ) and a decreased lignification rate, which translates into a low wood accumulation (Altesor et al, 1994 ; Reyes-Rivera et al, 2017 ). Some of these characteristics are more or less conspicuous depending on the phylogeny: in Opuntioideae and Cactoideae, two of the most recently derived subfamilies with a predominance of succulent forms, diverse wood configurations have been reported (cambial variants sensu ; Carlquist, 2001 ).…”

“…Some of these characteristics are more or less conspicuous depending on the phylogeny: in Opuntioideae and Cactoideae, two of the most recently derived subfamilies with a predominance of succulent forms, diverse wood configurations have been reported (cambial variants sensu ; Carlquist, 2001 ). These varies from monomorphic woods, with predominance of just one cell type, to polymorphic woods where similar proportions of more than one cell type, or alternatively, several changes in the predominant cell types occur (Mauseth and Plemons, 1995 ; Terrazas and Arias, 2002 ; Mauseth, 2006 ; Vázquez-Sánchez and Terrazas, 2011 ; Reyes-Rivera et al, 2017 ). In addition, there are species where the fibers, typical wood elements in woody dicots, are scarce or absent, instead occur an abundance of a very specialized cell type with limited extension of the secondary cell wall, called wide-band tracheid (WBT, Figure 1 ).…”

“…In addition, there are species where the fibers, typical wood elements in woody dicots, are scarce or absent, instead occur an abundance of a very specialized cell type with limited extension of the secondary cell wall, called wide-band tracheid (WBT, Figure 1 ). On the other hand, in Pereskioideae, the most ancestral subfamily with non-succulent stems, wood is completely fibrous, and in some species such as Pereskia lychnidiflora , WBTs are never present (Terrazas and Mauseth, 2002 ; Mauseth, 2004 ; Reyes-Rivera et al, 2017 ). An intriguing aspect is that lignin of many dimorphic woods is distinguished by being exceptionally rich in S units (97% in F. hamatacanthus , as determined by nitrobenzene oxidations) and by having a heterogeneous composition (Reyes-Rivera et al, 2015 ).…”

“…An intriguing aspect is that lignin of many dimorphic woods is distinguished by being exceptionally rich in S units (97% in F. hamatacanthus , as determined by nitrobenzene oxidations) and by having a heterogeneous composition (Reyes-Rivera et al, 2015 ). In contrast, the fibrous species show more homogeneous composition patterns (Reyes-Rivera et al, 2015 ) and lack KNOX transcription factors that are present in dimorphic species, factors related to dimorphic wood change (Reyes-Rivera et al, 2017 ). Thus, the different types of wood in Cactaceae are an excellent system to study the relationship between lignification and some evolutionary aspect of the growth form and other adaptive aspects concerning dimorphic wood structure.…”

“…Middle row: wood anatomy, transversal sections. Inferior row: wood macerations, obtained as described in Reyes-Rivera et al ( 2017 ). Fb, fibers; r, rays; v, vessels; VE, vessel elements; WBT, wide-band tracheids.…”