Natalia Pabón-Mora

Poppy APETALA1/FRUITFULL Orthologs Control Flowering Time, Branching, Perianth Identity, and Fruit Development

Several MADS box gene lineages involved in flower development have undergone duplications that correlate with the diversification of large groups of flowering plants. In the APETALA1 gene lineage, a major duplication coincides with the origin of the core eudicots, resulting in the euFUL and the euAP1 clades. Arabidopsis FRUITFULL (FUL) and APETALA1 (AP1) function redundantly in specifying floral meristem identity but function independently in sepal and petal identity (AP1) and in proper fruit development and determinacy (FUL). Many of these functions are largely conserved in other core eudicot euAP1 and euFUL genes, but notably, the role of APETALA1 as an “A-function” (sepal and petal identity) gene is thought to be Brassicaceae specific. Understanding how functional divergence of the core eudicot duplicates occurred requires a careful examination of the function of preduplication (FUL-like) genes. Using virus-induced gene silencing, we show that FUL-like genes in opium poppy (Papaver somniferum) and California poppy (Eschscholzia californica) function in axillary meristem growth and in floral meristem and sepal identity and that they also play a key role in fruit development. Interestingly, in opium poppy, these genes also control flowering time and petal identity, suggesting that AP1/FUL homologs might have been independently recruited in petal identity. Because the FUL-like gene functional repertoire encompasses all roles previously described for the core eudicot euAP1 and euFUL genes, we postulate subfunctionalization as the functional outcome after the major AP1/FUL gene lineage duplication event.

The Aquilegia FRUITFULL-like genes play key roles in leaf morphogenesis and inflorescence development

The APETALA1/FRUITFULL (AP1/FUL) MADS box transcription factors are best known for the role of AP1 in Arabidopsis sepal and petal identity, the canonical Axa0function of the ABC model of flower development. However, this gene lineage underwent multiple duplication events during angiosperm evolution, providing different taxa with unique gene complements. One such duplication correlates with the origin of the core eudicots, and produced the euAP1 and euFUL clades. Together, euAP1 and euFUL genes function in proper floral meristem identity and repression of axillary meristem growth. Independently, euAP1 genes function in floral meristem and sepal identity, whereas euFUL genes control phase transition, cauline leaf growth and fruit development. To investigate the impact of the core eudicot duplication on the functional diversification of this gene lineage, we studied the role of pre-duplication FUL-like genes in columbine (Aquilegia coerulea). Our results show that AqcFL1 genes are broadly expressed in vegetative and reproductive meristems, leaves and flowers. Virus-induced gene silencing of the loci results in plants with increased branching, shorter inflorescences with fewer flowers, and dramatic changes in leaf shape and complexity. However, aqcfl1 plants have normal flowers and fruits. Our results show that, in contrast to characterized AP1/FUL genes, the AqcFL1 loci are either genetically redundant or have been decoupled from the floral genetic program, and play a major role in leaf morphogenesis. We analyze the results in the context of the core eudicot duplication, and discuss the implications of our findings in terms of the genetic regulation of leaf morphogenesis in Aquilegia and other flowering plants.

Comparative anatomical and developmental analysis of dry and fleshy fruits of Solanaceae.

UNLABELLEDnnnnPREMISE OF THE STUDYnAn anatomical examination of dry and fleshy fruits within the Solanaceae was carried out to identify comparable stages throughout development as well as features exclusive to each type of fruit. We studied fruit development of Nicotiana and Petunia, which have the plesiomorphic capsular fruit; Solanum and Iochroma, characterized by a derived fleshy berry; Cestrum, an independent origin of a fleshy fruit; and Datura, a reversion to a dry fruit. •nnnMETHODSnPre- and postanthesis carpels and fruits of all species were collected, sectioned, stained, and examined using light microscopy. •nnnKEY RESULTSnComparable stages of carpel and fruit development were identified in all species. Furthermore, anatomical and developmental features were identified that characterize capsules in Solanaceae, including lack of increase in the number of pericarp cell layers, formation of a sclerified endocarp, and elongation of the epidermal cells of the placenta. Pericarps of fleshy fruits of the Solanoideae are characterized by abundant collenchyma, an increase in the number of cell layers, and a parenchymatous endocarp often expanding into the locules. Anatomical data show that early developmental stages of the fruit of Cestrum, a berry, are similar to the capsular fruits of Petunia and Nicotiana; similarly, Datura, one of the few capsular members of the Solanoideae, shares several anatomical features with closely related berried taxa. •nnnCONCLUSIONSnOntogenetically, all fleshy or all dry fruits do not necessarily share a common developmental ground plan. Independent evolution of fleshiness, sclerification, dryness, and dehiscence are discussed in a phylogenetic context.

Evolution of fruit development genes in flowering plants.

The genetic mechanisms regulating dry fruit development and opercular dehiscence have been identified in Arabidopsis thaliana. In the bicarpellate silique, valve elongation and differentiation is controlled by FRUITFULL (FUL) that antagonizes SHATTERPROOF1-2 (SHP1/SHP2) and INDEHISCENT (IND) at the dehiscence zone where they control normal lignification. SHP1/2 are also repressed by REPLUMLESS (RPL), responsible for replum formation. Similarly, FUL indirectly controls two other factors ALCATRAZ (ALC) and SPATULA (SPT) that function in the proper formation of the separation layer. FUL and SHP1/2 belong to the MADS-box family, IND and ALC belong to the bHLH family and RPL belongs to the homeodomain family, all of which are large transcription factor families. These families have undergone numerous duplications and losses in plants, likely accompanied by functional changes. Functional analyses of homologous genes suggest that this network is fairly conserved in Brassicaceae and less conserved in other core eudicots. Only the MADS box genes have been functionally characterized in basal eudicots and suggest partial conservation of the functions recorded for Brassicaceae. Here we do a comprehensive search of SHP, IND, ALC, SPT, and RPL homologs across core-eudicots, basal eudicots, monocots and basal angiosperms. Based on gene-tree analyses we hypothesize what parts of the network for fruit development in Brassicaceae, in particular regarding direct and indirect targets of FUL, might be conserved across angiosperms.

Homologies of the flower and inflorescence in the early-divergent grass Anomochloa (Poaceae)

PREMISE OF THE STUDYnThe grass subfamily Anomochlooideae is phylogenetically significant as the sister group to all other grasses. Thus, comparison of their structure with that of other grasses could provide clues to the evolutionary origin of these characters.nnnMETHODSnWe describe the structure, embryology, and development of the flower and partial inflorescence of the monotypic Brazilian grass Anomochloa marantoidea. We compare these features with those of other early-divergent grasses such as Pharus and Streptochaeta and closely related Poales such as Ecdeiocolea.nnnKEY RESULTSnAnomochloa possesses several features that are characteristic of Poaceae, notably a scutellum, a solid style, reduced stamen number, and an ovary with a single ovule that develops into a single indehiscent fruit. Interpretation of floral patterning in Anomochloa is problematic because the ramification pattern of the florets places the bracts and axes in unusual positions relative to the primary inflorescence axis. Our study indicates that there is a single abaxial carpel in Anomochloa, probably due to a cryptic type of pseudomonomery in Anomochloa that resembles the pseudomonomery of other grasses. On the other hand, the Anomochloa flower differs from the typical grass flower in lacking lodicules and possessing four stamens, in contrast with the tristaminate condition that characterizes many other grasses.nnnCONCLUSIONSnUsing the median part of the innermost bract as a locator, we tentatively homologize the inner bract of the Anomochloa partial inflorescence with the palea of other grasses. In this interpretation, the pattern of monosymmetry due to stamen suppression differs from that of Ecdeiocolea.

Floral Ontogeny of Telipogon spp. (Orchidaceae) and Insights on the Perianth Symmetry in the Family

Telipogon s.l. (i.e., including Hofmeisterella and Stellilabium) is a Neotropical epidendroid genus that has some species with an unusual tendency to develop an actinomorphic perianth; most species have the typical monosymmetric orchid perianth. The genus is nested in a clade that includes Pachyphyllum, Fernandezia, and Trichoceros, all of which consistently exhibit a monosymmetric perianth. The study of floral ontogeny in Telipogon shows that early and mid‐development is similar to that found in other orchids with monosymmetric perianth and that the acquisition of an actinomorphic perianth occurs late in development. On the basis of optimization of the mature polysymmetric perianth onto the phylogenetic analysis available for Telipogon, it has arisen independently several times within the genus; however, the polysymmetric perianth of Telipogon andicola and Telipogon nervosus (representing distant clades within the genus) is the result of the same developmental pathway. Conversely, a further comparison of floral development in other Telipogon spp., as well as in the closely related Fernandezia lanceolata and other distantly related orchids, indicates that the sequence of organ initiation is highly variable and that different ontogenetic pathways can lead to a monosymmetric perianth. Heterochrony during the development of the perianth has been proposed as one of the pivotal evolutionary processes that has enhanced a high‐specific radiation in the family. Our results in Telipogon agree with this statement.

Limited mitogenomic degradation in response to a parasitic lifestyle in Orobanchaceae

In parasitic plants, the reduction in plastid genome (plastome) size and content is driven predominantly by the loss of photosynthetic genes. The first completed mitochondrial genomes (mitogenomes) from parasitic mistletoes also exhibit significant degradation, but the generality of this observation for other parasitic plants is unclear. We sequenced the complete mitogenome and plastome of the hemiparasite Castilleja paramensis (Orobanchaceae) and compared them with additional holoparasitic, hemiparasitic and nonparasitic species from Orobanchaceae. Comparative mitogenomic analysis revealed minimal gene loss among the seven Orobanchaceae species, indicating the retention of typical mitochondrial function among Orobanchaceae species. Phylogenetic analysis demonstrated that the mobile cox1 intron was acquired vertically from a nonparasitic ancestor, arguing against a role for Orobanchaceae parasites in the horizontal acquisition or distribution of this intron. The C. paramensis plastome has retained nearly all genes except for the recent pseudogenization of four subunits of the NAD(P)H dehydrogenase complex, indicating a very early stage of plastome degradation. These results lend support to the notion that loss of ndh gene function is the first step of plastome degradation in the transition to a parasitic lifestyle.

Reassessing Inflorescence and Floral Morphology and Development in Hedyosmum (Chloranthaceae)

Hedyosmum (Chloranthaceae), one of the oldest angiosperm lineages, possesses some atypical reproductive features that remain poorly understood, including the inflorescence architecture, the stamen anatomy, and the perianth development around the allegedly inferior ovary. Our developmental survey of these characters with LM and SEM techniques showed that both staminate and carpellate partial inflorescences are indeterminate and suggests that each stamen corresponds to a single, ebracteolate flower. The tapetum is secretory and associated with orbicules; the connective apex is secretory, which—along with the reticulate pollen and the frequent visits of insects—suggests that entomophily should not be ruled out in Hedyosmum. The perianth is formed by three almost completely fused hypogynous tepals; the window is schyzogenous, unique among angiosperms, and according to the fossil record, it has been in the genus since the Early Cretaceous. Unlike any previous description, we found that the ovary is fully superior. The persistent perianth completely surrounds the fruit; in turn, they are tightly enclosed by the fused, acrescent, fleshy flower-subtending bracts, which appear to play a threefold role in protection, secretion, and dispersal.

Development and Morphology of Flowers in Loranthaceae

Premise of research.u2003Loranthaceae flowers exhibit exceedingly variable ground plan, size, and pollination syndromes. The homology of floral organs (especially the calyculus and the perianth), the evolutionary shifts from bisexual to unisexual flowers, and the trends in ovary and ovule reduction, primarily studied in Old World taxa, have been controversial. We investigate the development and morphoanatomy of early- and late-diverging Neotropical lineages with broad floral diversity to test organ homology and postulate floral plesiomorphies and apomorphies throughout the family. Methodology.u2003We examined eight species from six genera, all native to the Colombian Andes. Standard LM and SEM methods were used. Pivotal results.u2003All species studied exhibit bisexual flowers, but partial or total stamen sterilization was observed in the small-flowered Passovia pyrifolia and Peristethium archeri. All flowers examined possess an irregular calyx developed from a ring primordium, distinct from the four to seven petals initially free but postgenitally fused, and four to seven epipetalous stamens. Additionally, a cupular pedicel is present, either free from the calyx in Aetanthus and Psittacanthus or fused to the calyx in Passovia. Polysporangiate anthers were detected in Aetanthus mutisii; they dehisce prior to anthesis, which suggests cleistogamy. The ovary is six- or seven-chambered in Gaiadendron punctatum, but it is variously reduced or even solid in the remaining taxa. Conclusions.u2003Plesiomorphies in the family include sessile, bisexual flowers lacking a cupular pedicel; an irregularly developed, distinct calyx; free, simultaneous petal primordia; versatile and tetrasporangiate anthers; and an ovary with six or seven locules and mamelons. The cupular pedicel is apomorphic in some Psittacanthinae genera. Other apomorphies include the basifixed, polysporangiate anthers with preanthetic dehiscence in A. mutisii. Unisexual flowers are homoplasious and linked to small-flowered taxa; anther sterilization occurs by either reduction in the number of sporangia or a proliferating endothecium. The modification of the ovary across Loranthaceae likely reflects pseudomonomery.

Leaf Development, Metamorphic Heteroblasty and Heterophylly in Berberis s. l. (Berberidaceae)

Shoot development of temperate and tropical members of Berberis s. l. was examined in order to assess: (1) the homology of the spines along the long shoots and the foliage leaves that form on the short shoots; (2) the occurrence of heterophylly and/or heteroblasty in the genus; and (3) the structural correspondence between cataphylls, spines, and foliage leaves. The 1-5-armed spines have been interpreted as modified compound leaves lacking stipules, as a modified lamina (central spine) with stipules (lateral spines), or less often, as transformed branches, or as epidermal outgrowths. On the other hand, the foliage leaves of the short shoots have been interpreted as leaflets of palmately compound leaves. Our results indicate that there are three distinct leaf types per node: (1) Leaves modified in spines spirally arranged in long shoots; (2) foliage, expanded leaves densely arranged in short shoots; and (3) cataphylls protecting axillary buds. The spines are leaf homologs with a clear distinction between the leaf base with stipules, and a laminar portion modified into the 1-5-armed spine; the lateral spines are not stipules as they arise from the marginal meristem of the laminar portion, and not from the leaf base. The foliage leaves also have stipules flanking the leaf base. Both spiny leaves and foliage leaves develop an articulation between the base and the laminar portion. Cataphylls of the short shoots of Berberis s. str. and those of the reproductive short shoots of Mahonia correspond to the entire leaf base, but those of the renewal (vegetative) shoots of Mahonia are spiny and have an odd vestigial pinnately compound lamina. Heterochrony due to ontogenetic truncation caused by the formation of the terminal inflorescence at the apex of the short shoots could be responsible for the lack of petiole/lamina differentiation in the foliage leaves. The spiny long-shoot/foliose short-shoot system of branching in Berberis s. str. appears to be genetically and phylogenetically fixed and not environment-dependent. This represents a clear example of metamorphic heteroblasty sensu Zotz et al. (Botanical Review 77:109–151, 2011) with further occurrence of heterophylly along the short shoots.