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Research Article

Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape

Yasunori Ichihashi, José Antonio Aguilar-Martínez, Moran Farhi, Daniel H. Chitwood, Ravi Kumar, Lee V. Millon, Jie Peng, Julin N. Maloof, and Neelima R. Sinha
PNAS June 24, 2014 111 (25) E2616-E2621; first published June 9, 2014; https://doi.org/10.1073/pnas.1402835111
Yasunori Ichihashi
aDepartment of Plant Biology,
bCenter for Sustainable Resource Science, RIKEN, Yokohama, Kanagawa 230-0045, Japan
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José Antonio Aguilar-Martínez
aDepartment of Plant Biology,
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Moran Farhi
aDepartment of Plant Biology,
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Daniel H. Chitwood
aDepartment of Plant Biology,
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Ravi Kumar
aDepartment of Plant Biology,
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Lee V. Millon
cSchool of Veterinary Medicine, and
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Jie Peng
dDepartment of Statistics, University of California, Davis, CA 95616; and
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Julin N. Maloof
aDepartment of Plant Biology,
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Neelima R. Sinha
aDepartment of Plant Biology,
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  • For correspondence: nrsinha@ucdavis.edu
  1. Edited by Philip N. Benfey, Duke University, Durham, NC, and approved May 14, 2014 (received for review February 14, 2014)

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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.

  • Solanum species
  • RNA-seq
  • bioinformatics

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.

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Gene network module regulating leaf shape
Yasunori Ichihashi, José Antonio Aguilar-Martínez, Moran Farhi, Daniel H. Chitwood, Ravi Kumar, Lee V. Millon, Jie Peng, Julin N. Maloof, Neelima R. Sinha
Proceedings of the National Academy of Sciences Jun 2014, 111 (25) E2616-E2621; DOI: 10.1073/pnas.1402835111

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Gene network module regulating leaf shape
Yasunori Ichihashi, José Antonio Aguilar-Martínez, Moran Farhi, Daniel H. Chitwood, Ravi Kumar, Lee V. Millon, Jie Peng, Julin N. Maloof, Neelima R. Sinha
Proceedings of the National Academy of Sciences Jun 2014, 111 (25) E2616-E2621; DOI: 10.1073/pnas.1402835111
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