The evolution of spinnable cotton fiber entailed prolonged development and a novel metabolism

Abstract

A central question in evolutionary biology concerns the developmental processes by which new phenotypes arise. An exceptional example of evolutionary innovation is the single-celled seed trichome in Gossypium ("cotton fiber"). We have used fiber development in Gossypium as a system to understand how morphology can rapidly evolve. Fiber has undergone considerable morphological changes between the short, tightly adherent fibers of G. longicalyx and the derived long, spinnable fibers of its closest relative, G. herbaceum, which facilitated cotton domestication. We conducted comparative gene expression profiling across a developmental time-course of fibers from G. longicalyx and G. herbaceum using microarrays with approximately 22,000 genes. Expression changes between stages were temporally protracted in G. herbaceum relative to G. longicalyx, reflecting a prolongation of the ancestral developmental program. Gene expression and GO analyses showed that many genes involved with stress responses were upregulated early in G. longicalyx fiber development. Several candidate genes upregulated in G. herbaceum have been implicated in regulating redox levels and cell elongation processes. Three genes previously shown to modulate hydrogen peroxide levels were consistently expressed in domesticated and wild cotton species with long fibers, but expression was not detected by quantitative real time-PCR in wild species with short fibers. Hydrogen peroxide is important for cell elongation, but at high concentrations it becomes toxic, activating stress processes that may lead to early onset of secondary cell wall synthesis and the end of cell elongation. These observations suggest that the evolution of long spinnable fibers in cotton was accompanied by novel expression of genes assisting in the regulation of reactive oxygen species levels. Our data suggest a model for the evolutionary origin of a novel morphology through differential gene regulation causing prolongation of an ancestral developmental program.

Figure 1. Evolutionary History of Cotton in Relation to the Current Study

(A) Evolutionary history of diploid and tetraploid Gossypium species groups (n = 13 and 26, respectively), as inferred from multiple molecular datasets [11,13], indicating sister-taxon relationship between the F- and A- genomes. F-, G. longicalyx (short fibers); A-, G. herbaceum (long fibers). (B) Microarray experimental loop-design for detecting gene expression changes during the development of A- and F-genome fibers. Arrows denote dyes that were used in each of the hybridizations (tails, Cy3; arrow heads, Cy5).

Figure 2. Summary of the Number of Genes Differentially Expressed between Adjacent Time-Points during Fiber Development (FDR < 0.05)

Figure 3. Quantitative Real-Time PCR Analyses of Three Candidate Genes Controlling H₂O₂ Levels

Gossypium species investigated were G. herbaceum (A1), G. longicalyx (F) (left panel); G. hirsutum var TM1 (TM1), G. hirsutum var yucatanense (YUC), G. arboreum (A2), and G. raimondii (D5) (right panel). Each point on the graph represents the mean of three biological replications.

Figure 4. An Evolutionary and Development Model Describing Processes That Lead to the Formation of Spinnable Fiber