Renata Reinheimer

Inflorescence, spikelet, and floral development in Panicum maximum and Urochloa plantaginea (Poaceae)

Inflorescence development in Panicum maximum and Urochloa plantaginea was comparatively studied with scanning electron and light microscopy to test the transfer of P. maximum to Urochloa and to look for developmental features applicable to future cladistic studies of the phosphoenol pyruvate carboxykinase (PCK) subtype of C(4) photosynthesis clade (P. maximum and some species of Brachiaria, Chaetium, Eriochloa, Melinis, and Urochloa). Eleven developmental features not discernable in the mature inflorescence were found: direction of branch differentiation; origins of primary branches; apical vs. intercalary development of the main axis; direction of spikelet differentiation; direction of glume, lemma and palea differentiation; position of the lower glume (in some cases); size of the floret meristem; pattern of distal floret development; pattern of gynoecium abortion; differential pollen development between proximal and distal floret; and glume elongation. Inflorescence homologies between P. maximum and U. plantaginea are also clarified. Panicum maximum and U. plantaginea differ not only in their mature inflorescence structure but also in eight fundamental developmental features that exclude P. maximum from Urochloa. The following developmental events are related to sex expression: size of floret meristem, gynoecium abortion, pollen development delay in the proximal floret, glume elongation and basipetal floret maturation at anthesis.

Diversification of inflorescence development in the PCK clade (Poaceae: Panicoideae: Paniceae).

In grasses, inflorescence diversification and its correlation with species evolution are intriguing and not well understood. Part of this problem lies in our lack of comprehension about the inflorescence morphological complexity of grasses. We focused our study on the PCK clade (named for phosphoenol pyruvate carboxykinase), a well-supported monophyletic group for which the relationships among its taxa are not well resolved. Interestingly, the PCK clade has an extensive diversity of adult inflorescence forms. A comparative developmental approach can help us to understand the basis of such morphological differences as well as provide characters that can be used in phylogenetic studies of the group. Using SEM studies, we demonstrate that inflorescence morphology in this clade is even more complex than what is typically observed in adult forms. We describe a number of new characters, and some classical features previously used for taxonomic purposes are redefined on the basis of development. We also define four morphological groups combining adult inflorescence form and development, and we discuss some of the evolutionary aspects of inflorescence diversification in the PCK clade. Taxonomic delimitation among genera in the PCK clade remains confusing and unclear where molecular and morphological studies support different classifications.

Macroevolution of panicoid inflorescences: a history of contingency and order of trait acquisition.

BACKGROUND AND AIMS Inflorescence forms of panicoid grasses (Panicoideae s.s.) are remarkably diverse and they look very labile to human eyes; however, when performing a close inspection one can identify just a small subset of inflorescence types among a huge morphospace of possibilities. Consequently, some evolutionary constraints have restricted, to some extent, the diversification of their inflorescence. Developmental and genetic mechanisms, the photosynthetic type and plant longevity have been postulated as candidate constraints for angiosperms and panicoids in particular; however, it is not clear how these factors operate and which of these have played a key role during the grass inflorescence evolution. To gain insight into this matter the macroevolutionary aspects of panicoid inflorescences are investigated. METHODS The inflorescence aspect (lax versus condensed), homogenization, truncation of the terminal spikelet, plant longevity and photosynthetic type were the traits selected for this study. Maximum likelihood and Bayesian Markov chain Monte Carlo methods were used to test different models of evolution and to evaluate the existence of evolutionary correlation among the traits. Both, models and evolutionary correlation were tested and analysed in a phylogenetic context by plotting the characters on a series of trees. For those cases in which the correlation was confirmed, test of contingency and order of trait acquisition were preformed to explore further the patterns of such co-evolution. KEY RESULTS The data reject the independent model of inflorescence trait evolution and confirmed the existence of evolutionary contingency. The results support the general trend of homogenization being a prerequisite for the loss of the terminal spikelet of the main axis. There was no evidence for temporal order in the gain of homogenization and condensation; consequently, the homogenization and condensation could occur simultaneously. The correlation between inflorescence traits with plant longevity and photosynthetic type is not confirmed. CONCLUSIONS The findings indicate that the lability of the panicoid inflorescence is apparent, not real. The results indicate that the history of the panicoids inflorescence is a combination of inflorescence trait contingency and order of character acquisition. These indicate that developmental and genetic mechanisms may be important constraints that have limited the diversification of the inflorescence form in panicoid grasses.

Evolution and Development of the Spikelet and Flower of Rhynchospora (Cyperaceae)

Premise of research. Rhynchospora, one of the biggest genera of sedges, displays several spikelet and flower modifications and is one of a few genera where the pollination strategy changes from wind to insect pollination; however, the mechanisms that have promoted such diversity in the genus are unknown. We have performed a comparative study of spikelet and flower development of Rhynchospora from an evolutionary perspective to get insight into the bases of spikelet and flower evolution. Particularly, we investigate correlations between the change from wind to insect pollination that occur in the genus and the spikelet and flower traits. Methodology. The spikelet and flower development of nine species of Rhynchospora were studied using SEM images. Parsimony, maximum likelihood, and Bayesian reconstruction analyses were conducted to evaluate the evolutionary history of flower and spikelet developmental programs. Pivotal results. We identified seven morphological and developmental traits that vary among Rhynchospora species; ancestral character reconstructions show that the spikelet and flower morphology and their developmental pathways support the diversification of Rhynchospora lineages. Conclusions. Our results suggest that the evolution of spikelet and flower developmental programs in Rhynchospora may be related to the evolution of its pollination type and mating system. The evolution toward a bisexual spikelet and flowers in which the androecium develops faster than the gynoecium may represent important steps for the transition from a wind- to insect-pollination system. In addition, we found new traits of spikelets and flowers that may help to distinguish natural groups within Rhynchospora.

Changes in Floret Development Patterns That May Correlate with Sex Determination in the PCK Clade (Poaceae)

We investigated changes in floral developmental patterns and sex determination in the PCK (phosphoenolpyruvate carboxykinase) clade using a comparative approach and SEM. We identified variation in patterns of floral development that may be correlated with sex determination. Nine different patterns of floret development were identified, based on sex of the lower floret, sequence of stamen development, and rate of glume and lemma differentiation. Although staminate florets are always formed by the abortion of the gynoecium, the timing of abortion differs among species. Similarly, the formation of sterile lower florets showed different pathways that may operate at the level of floral meristem or organ identity. Finally, we discuss several reasons why patterns described for maize and closely related species may not be easily extrapolated to other grasses.

Macro-Climatic Distribution Limits Show Both Niche Expansion and Niche Specialization among C4 Panicoids.

Grasses are ancestrally tropical understory species whose current dominance in warm open habitats is linked to the evolution of C4 photosynthesis. C4 grasses maintain high rates of photosynthesis in warm and water stressed environments, and the syndrome is considered to induce niche shifts into these habitats while adaptation to cold ones may be compromised. Global biogeographic analyses of C4 grasses have, however, concentrated on diversity patterns, while paying little attention to distributional limits. Using phylogenetic contrast analyses, we compared macro-climatic distribution limits among ~1300 grasses from the subfamily Panicoideae, which includes 4/5 of the known photosynthetic transitions in grasses. We explored whether evolution of C4 photosynthesis correlates with niche expansions, niche changes, or stasis at subfamily level and within the two tribes Paniceae and Paspaleae. We compared the climatic extremes of growing season temperatures, aridity, and mean temperatures of the coldest months. We found support for all the known biogeographic distribution patterns of C4 species, these patterns were, however, formed both by niche expansion and niche changes. The only ubiquitous response to a change in the photosynthetic pathway within Panicoideae was a niche expansion of the C4 species into regions with higher growing season temperatures, but without a withdrawal from the inherited climate niche. Other patterns varied among the tribes, as macro-climatic niche evolution in the American tribe Paspaleae differed from the pattern supported in the globally distributed tribe Paniceae and at family level.

Insights into panicoid inflorescence evolution

Inflorescence forms can be described by different combinatorial patterns of meristem fates (indeterminate versus determinate). In theory, the model predicts that any combination is possible. Whether this is true for grasses is unknown. In this paper, the subfamily Panicoideae s.s. (panicoid grasses) was chosen as the model group to investigate this aspect of grass inflorescence evolution. We have studied the inflorescence morphology of 201 species to complement information available in the literature. We have identified the most recurrent inflorescence types and character states among panicoids. Using multivariate approaches, we have indentified correlations among different inflorescence character states. By phylogenetic reconstruction methods we have inferred the patterns of panicoid inflorescence evolution. Our results demonstrate that not all theoretical combinatorial patterns of variation are found in panicoids. The fact that each panicoid lineage has a unique pattern of inflorescence evolution adds an evolutionary component to combinatorial model.

Diversity, systematics, and evolution of Cynodonteae inflorescences (Chloridoideae – Poaceae)

The species of the Cynodonteae tribe show great morphological diversity in their reproductive structures. Previous studies where inflorescences were comparatively analysed in the context of phylogeny have shown that although grass inflorescences seem to be excessively variable, there are certain aspects of inflorescences that store relevant information on the evolution and systematics in Poaceae. We have analysed and compared the inflorescence structures of species belonging to the Hilariinae, Monanthochloinae, Scleropogoninae, and Muhlenbergiinae subtribes. Considering the most relevant morphological characters, the most recurrent types of inflorescences in the lineage were determined by means of a principal coordinates analysis. To understand the evolution of inflorescence morphology, ancestral reconstructions of inflorescence characters were performed using the Bayesian inference method. The results obtained demonstrate that the processes of homogenization and truncation might account for the diversity observed in adult inflorescences. Five different types of inflorescences were identified out of 36 theoretical possibilities. Amongst these, inflorescence type 1 (panicle of spikelets, with a terminal spikelet, non-homogenized, and bearing third- or higher-order branches) was found to be the most frequent in the studied group. Ancestral reconstructions of morphological characters allowed us to suggest that the ancestor of the group might have had an inflorescence with the form of a raceme of spikelets, non-truncated and bearing first-order branches. More complex inflorescences bearing no terminal spikelets and having branches of higher order might have diverged this lineage.

Evolutionary history of HOMEODOMAIN LEUCINE ZIPPER transcription factors during plant transition to land

Plant transition to land required several regulatory adaptations. The mechanisms behind these changes remain unknown. Since the evolution of transcription factors (TFs) families accompanied this transition, we studied the HOMEODOMAIN LEUCINE ZIPPER (HDZ) TF family known to control key developmental and environmental responses. We performed a phylogenetic and bioinformatics analysis of HDZ genes using transcriptomic and genomic datasets from a wide range of Viridiplantae species. We found evidence for the existence of HDZ genes in chlorophytes and early-divergent charophytes identifying several HDZ members belonging to the four known classes (I-IV). Furthermore, we inferred a progressive incorporation of auxiliary motifs. Interestingly, most of the structural features were already present in ancient lineages. Our phylogenetic analysis inferred that the origin of classes I, III, and IV is monophyletic in land plants in respect to charophytes. However, class IIHDZ genes have two conserved lineages in charophytes and mosses that differ in the CPSCE motif. Our results indicate that the HDZ family was already present in green algae. Later, the HDZ family expanded accompanying critical plant traits. Once on land, the HDZ family experienced multiple duplication events that promoted fundamental neo- and subfunctionalizations for terrestrial life.