Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule‐bearing organs

Abstract

SummaryReproductive organs in seed plants are morphologically divergent and their evolutionary history is often unclear. The mechanisms controlling their development have been extensively studied in angiosperms but are poorly understood in conifers and other gymnosperms. Here, we address the molecular control of seed cone development in Norway spruce, Picea abies.We present expression analyses of five novel MADS-box genes in comparison with previously identified MADS and LEAFY genes at distinct developmental stages. In addition, we have characterized the homeotic transformation from vegetative shoot to female cone and associated changes in regulatory gene expression patterns occurring in the acrocona mutant.The analyses identified genes active at the onset of ovuliferous and ovule development and identified expression patterns marking distinct domains of the ovuliferous scale. The reproductive transformation in acrocona involves the activation of all tested genes normally active in early cone development, except for an AGAMOUS-LIKE6/SEPALLATA (AGL6/SEP) homologue. This absence may be functionally associated with the nondeterminate development of the acrocona ovule-bearing scales.Our morphological and gene expression analyses give support to the hypothesis that the modern cone is a complex structure, and the ovuliferous scale the result of reductions and compactions of an ovule-bearing axillary short shoot in cones of Paleozoic conifers.

From leaf and branch into a flower: Magnolia tells the story

“…The Unifying Theory, a hypothesis founded on a Jurassic plant with free central placentation, dissects a carpel into an ovule-bearing shoot (placenta) and its enclosing foliar structure (Wang 2010). This treatment was suggested previously by the Gonophyll Theory (Melville 1962) and is compatible using data from various fields of botany, including development, morphology, anatomy, gene function analysis, and systematic analysis (Herr 1995; Rounsley et al 1995; Hickey and Taylor 1996; Skinner et al 2004; Dreni et al 2007; Doyle 2008; Zheng et al 2010; Carlsbecker et al 2013). If this treatment is correct, a logical inference is that there should be vascular bundles of radial symmetry (namely, amphicribral bundles) in the placenta.…”

Evolution of fruit development genes in flowering plants

“…BS for this duplication is low (<50), and the position of the AG/SHP monocot clade is variable (retested in parsimony analyses, data not shown), nevertheless the two main resulting clades have BS of 82 and within each clade, relationships among genes are mostly consistent with the phylogenetic relationships of the sampled taxa (APG, 2009). This contrasts with the single copy C and D class genes found in gymnosperms (Kramer et al, 2004; Carlsbecker et al, 2013). They appear to be paraphyletic with respect to the angiosperm C and D lineages, but the three clades that they form have strong supports (Figure 5).…”

“…Although comparative studies, are needed to understand the role of AGAMOUS homologs in early diverging flowering plants, the conserved expression of AG/STK homologs in gymnosperms (Jager et al, 2003; Carlsbecker et al, 2013) suggest that the ancestral role of the gene lineage includes ovule identity. Such a role was then kept as part of the functional repertoire in STK genes, and AG genes were likely recruited first for carpel identity in early diverging angiosperms and later on for fruit development in core eudicots (Kramer et al, 2004).…”

“…In addition, RPL is also known to have pleiotropic effects in plant development particularly in various plant meristems (Byrne et al, 2003; Roeder et al, 2003; Smith and Hake, 2003; Bhatt et al, 2004; Hake et al, 2004; Smith et al, 2004). Many of the MADS-box protein homologs present in basal angiosperms, monocots, and basal eudicots play pleiotropic functions that include floral meristem and perianth identity (e.g., AP1/FUL proteins; Bowman et al, 1993; Gu et al, 1998; Ferrándiz et al, 2000b; Berbel et al, 2001, 2012; Murai et al, 2003; Pabón-Mora et al, 2012, 2013b), ovule, stamen, and carpel identity (STK/AG proteins; Jager et al, 2003; Yellina et al, 2010; Hands et al, 2011; Carlsbecker et al, 2013). …”

“…Outgroup sequences used for the APETALA1 / FRUITFULL genes include AGAMOUS Like-6 genes from several angiosperms (Litt and Irish, 2003; Zahn et al, 2005; Viaene et al, 2010). For AGAMOUS/SEEDSTICK genes the outgroup includes AGAMOUS Like-12 sequences from several angiosperms (Becker and Theissen, 2003; Carlsbecker et al, 2013). For HECATE3 / INDEHISCENT genes outgroup sequences include the closely related AtbHLH52 and AtbHLH53 from Arabidopsis as well has HECATE1 and HECATE2 from other angiosperms (Heim et al, 2003; Toledo-Ortiz et al, 2003).…”