Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton ( Gossypium )

Abstract

Cotton is remarkable among our major crops in that four species were independently domesticated, two allopolyploids and two diploids. In each case thousands of years of human selection transformed sparsely flowering, perennial shrubs into highly productive crops with seeds bearing the vastly elongated and abundant single-celled hairs that comprise modern cotton fiber. The genetic underpinnings of these transformations are largely unknown, but comparative gene expression profiling experiments have demonstrated up-regulation of profilin accompanying domestication in all three species for which wild forms are known. Profilins are actin monomer binding proteins that are important in cytoskeletal dynamics and in cotton fiber elongation. We show that Gossypium diploids contain six profilin genes (GPRF1-GPRF6), located on four different chromosomes (eight chromosomes in the allopolyploid). All but one profilin (GPRF6) are expressed during cotton fiber development, and both homeologs of GPRF1-GPRF5 are expressed in fibers of the allopolyploids. Remarkably, quantitative RT-PCR and RNAseq data demonstrate that GPRF1-GPRF5 are all up-regulated, in parallel, in the three independently domesticated cottons in comparison with their wild counterparts. This result was additionally supported by iTRAQ proteomic data. In the allopolyploids, there This usage of novel should be fine, since it refers to a novel evolutionary process, not a novel discovery has been novel recruitment of the sixth profilin gene (GPRF6) as a result of domestication. This parallel up-regulation of an entire gene family in multiple species in response to strong directional selection is without precedent and suggests unwitting selection on one or more upstream transcription factors or other proteins that coordinately exercise control over profilin expression.polyploidy | crop evolution | fiber | directional selection

Comparative Proteomic Analysis of Cotton Fiber Development and Protein Extraction Method Comparison in Late Stage Fibers

“…Plant cell morphology is largely determined by the highly dynamic actin cytoskeleton [55]. In this study, we found that cytoskeletal proteins were highly differentially regulated during fiber development, which included actin and actin binding proteins profilin and annexin.…”

“…In this study, we identified multiple cytoskeletal-related proteins that were differentially regulated, including the actin binding proteins, profilin and actin-depolymerizing factor (ADF). Profilins have been found to be expressed during early cotton fiber development [53,54,55], and when overexpressed in transgenic tobacco cells, they produced an elongated cell with thicker and longer microfilament cables [54,55]. We found that an isoform of profilin (A0A0B0PF49) was downregulated during secondary wall deposition (25 dpa) when compared to an earlier fiber development stage (15 dpa), while actin depolymerizing factor 7 (A1XJ44) was found to be upregulated in 15 dpa when compared to 10 dpa and downregulated in 25 dpa fiber when compared to 15 dpa.…”

“…Wang et al found that expression of a profilin family member (GhPFN2) was significantly induced during the period of rapid fiber elongation and secondary wall synthesis [55,69]. Another important regulator of actin dynamics, annexin was found to be downregulated in 15 dpa and 25 dpa fiber.…”

Breeding Open-Pollinated, Hybrid and Transgenic Outcrossing Species

“…The domesticated cottons, which were independently domesticated, show the lint or the spinnable seed fibers that result from human selection. Comparative gene expression-profiling experiments demonstrated upregulation of profilin accompanying domestication in the species for which wild relatives are known (Bao et al 2011). Profilins are actin monomer binding proteins involved in cytoskeletal dynamics and in cotton fiber elongation.…”

Genome-wide identification and expression analysis of Gossypium RING-H2 finger E3 ligase genes revealed their roles in fiber development, and phytohormone and abiotic stress responses

“…The ATL family of RING finger proteins, which contain a RING-H2 domain, was first identified in Arabidopsis (Salinas-Mondragon et al 1999) and later found to be widely distributed in all plants, including 80 and 121 ATL genes in Arabidopsis and rice, respectively (Serrano et al 2006). Cotton is the world's largest and most vital source of renewable textile fiber (Bao et al 2011). G. arboreum and G. raimondii underwent whole-genome duplication events about 16.6 million years ago (Mya), and G. hirsutum (allotetraploid) emerged from hybridizations of A or D diploid ancestral species nearly 1.5 Mya (Li et al 2015).…”