Evolution of Catkins: Inflorescence Morphology of Selected Salicaceae in an Evolutionary and Developmental Context

Fossil data have been interpreted as indicating that Late Cretaceous tropical forests were open and dry adapted and that modern closed-canopy rain forest did not originate until after the Cretaceous-Tertiary (K/T) boundary. However, some mid-Cretaceous leaf floras have been interpreted as rain forest. Molecular divergence-time estimates within the clade Malpighiales, which constitute a large percentage of species in the shaded, shrub, and small tree layer in tropical rain forests worldwide, provide new tests of these hypotheses. We estimate that all 28 major lineages (i.e., traditionally recognized families) within this clade originated in tropical rain forest well before the Tertiary, mostly during the Albian and Cenomanian (112-94 Ma). Their rapid rise in the mid-Cretaceous may have resulted from the origin of adaptations to survive and reproduce under a closed forest canopy. This pattern may also be paralleled by other similarly diverse lineages and supports fossil indications that closed-canopy tropical rain forests existed well before the K/T boundary. This case illustrates that dated phylogenies can provide an important new source of evidence bearing on the timing of major environmental changes, which may be especially useful when fossil evidence is limited or controversial.

All species of the genus Populus (poplar, aspen) are dioecious, suggesting an ancient origin of this trait. Despite some empirical counter examples, theory suggests that nonrecombining sex-linked regions should quickly spread, eventually becoming heteromorphic chromosomes. In contrast, we show using whole-genome scans that the sex-associated region in Populus trichocarpa is small and much younger than the age of the genus. This indicates that sex determination is highly labile in poplar, consistent with recent evidence of 'turnover' of sex-determination regions in animals. We performed whole-genome resequencing of 52 P. trichocarpa (black cottonwood) and 34 Populus balsamifera (balsam poplar) individuals of known sex. Genomewide association studies in these unstructured populations identified 650 SNPs significantly associated with sex. We estimate the size of the sex-linked region to be ~100 kbp. All SNPs significantly associated with sex were in strong linkage disequilibrium despite the fact that they were mapped to six different chromosomes (plus 3 unmapped scaffolds) in version 2.2 of the reference genome. We show that this is likely due to genome misassembly. The segregation pattern of sex-associated SNPs revealed this to be an XY sex-determining system. Estimated divergence times of X and Y haplotype sequences (6-7 Ma) are much more recent than the divergence of P. trichocarpa (poplar) and Populus tremuloides (aspen). Consistent with this, in P. tremuloides, we found no XY haplotype divergence within the P. trichocarpa sex-determining region. These two species therefore have a different genomic architecture of sex, suggestive of at least one turnover event in the recent past.

Flower production and crop yields are highly influenced by the architectures of inflorescences. In the compound inflorescences of tomato and related nightshades (Solanaceae), new lateral inflorescence branches develop on the flanks of older branches that have terminated in flowers through a program of plant growth known as "sympodial." Variability in the number and organization of sympodial branches produces a remarkable array of inflorescence architectures, but little is known about the mechanisms underlying sympodial growth and branching diversity. One hypothesis is that the rate of termination modulates branching. By performing deep sequencing of transcriptomes, we have captured gene expression dynamics from individual shoot meristems in tomato as they gradually transition from a vegetative state to a terminal flower. Surprisingly, we find thousands of age-dependent expression changes, even when there is little change in meristem morphology. From these data, we reveal that meristem maturation is an extremely gradual process defined molecularly by a "meristem maturation clock." Using hundreds of stage-enriched marker genes that compose this clock, we show that extreme branching, conditioned by loss of expression of the COMPOUND INFLORESCENCE gene, is driven by delaying the maturation of both apical and lateral meristems. In contrast, we find that wild tomato species display a delayed maturation only in apical meristems, which leads to modest branching. Our systems genetics approach reveals that the program for inflorescence branching is initiated surprisingly early during meristem maturation and that evolutionary diversity in inflorescence architecture is modulated by heterochronic shifts in the acquisition of floral fate.