Atmospheric methane levels increased over geological formations in Northern Siberia following a heat wave in 2020, suggesting that permafrost thaw releases methane from reservoirs.
Image credit: Wikimedia Commons.
Edited by Philip N. Benfey, Duke University, Durham, NC, and approved May 14, 2014 (received for review February 14, 2014)
Significance
Ever since Darwin’s pioneering research, a major challenge in biology has been to understand the genetic basis of morphological evolution. Utilizing the natural variation in leaf morphology between tomato and two related wild species, we identified a gene network module that leads to a dynamic rewiring of interactions in the whole leaf developmental gene regulatory network. Our work experimentally validates the hypothesis that peripheral regions of network, rather than network hubs, are more likely to contribute to evolutionary innovations. Our data also suggest that, likely due to their bottleneck location in the network, the regulation in KNOX homeobox genes was repeatedly manipulated to generate natural variation in leaf shape.
Abstract
Despite a long-standing interest in the genetic basis of morphological diversity, the molecular mechanisms that give rise to developmental variation are incompletely understood. Here, we use comparative transcriptomics coupled with the construction of gene coexpression networks to predict a gene regulatory network (GRN) for leaf development in tomato and two related wild species with strikingly different leaf morphologies. The core network in the leaf developmental GRN contains regulators of leaf morphology that function in global cell proliferation with peripheral gene network modules (GNMs). The BLADE-ON-PETIOLE (BOP) transcription factor in one GNM controls the core network by altering effective concentration of the KNOTTED-like HOMEOBOX gene product. Comparative network analysis and experimental perturbations of BOP levels suggest that variation in BOP expression could explain the diversity in leaf complexity among these species through dynamic rewiring of interactions in the GRN. The peripheral location of the BOP-containing GNM in the leaf developmental GRN and the phenotypic mimics of evolutionary diversity caused by alteration in BOP levels identify a key role for this GNM in canalizing the leaf morphospace by modifying the maturation schedule of leaves to create morphological diversity.
Footnotes
↵1Present address: Donald Danforth Plant Science Center, St. Louis, MO 63132.
↵2Present address: Novozymes, Inc., Davis, CA 95618.
- ↵3To whom correspondence should be addressed. E-mail: nrsinha{at}ucdavis.edu.
Author contributions: Y.I. and N.R.S. designed research; Y.I., J.A.A.-M., M.F., D.H.C., R.K., and L.V.M. performed research; J.P. and J.N.M. contributed new reagents/analytic tools; Y.I. analyzed data; and Y.I. and N.R.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive (http://trace.ncbi.nlm.nih.gov/Traces/sra/) (accession nos. SRP041563 and SRP041731).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1402835111/-/DCSupplemental.
Freely available online through the PNAS open access option.
Gene network module regulating leaf shape
Article Classifications
- Biological Sciences
- Plant Biology
Sign up for Article Alerts
Jump to section
You May Also be Interested in
Pottery, burnt clay, and burnt flint from Jordan dated from 7752 BCE to 5069 BCE yielded a record of variations in Earth’s magnetic field strength during the Neolithic period.
Image credit: Thomas E. Levy.
Mechanics of ant tunneling could inspire the development of improved robotic mining techniques.
Image credit: Jose E. Andrade and David R. Miller (California Institute of Technology, Pasadena, CA).
New observations now allow the seemingly impossible: measuring the speeds of some stars along the line of sight without ascertaining their Doppler shifts.
Image credit: NASA, H.E. Bond, and E. Nelan (Space Telescope Science Institute, Baltimore, MD); M. Barstow and M. Burleigh (University of Leicester, UK); and J.B. Holberg (University of Arizona, Tucson, AZ).
Researchers found a gene that could pave the way toward modifying crops so that they produce stable hybrid seed lines with desirable traits.
Image credit: Aleksandr Ozerov.