TY - JOUR
T1 - The strength and pattern of natural selection on gene expression in rice
AU - Groen, Simon C.
AU - Ćalić, Irina
AU - Joly-Lopez, Zoé
AU - Platts, Adrian E.
AU - Choi, Jae Young
AU - Natividad, Mignon
AU - Dorph, Katherine
AU - Mauck, William M.
AU - Bracken, Bernadette
AU - Cabral, Carlo Leo U.
AU - Kumar, Arvind
AU - Torres, Rolando O.
AU - Satija, Rahul
AU - Vergara, Georgina
AU - Henry, Amelia
AU - Franks, Steven J.
AU - Purugganan, Michael D.
N1 - Funding Information:
Acknowledgements We thank B. U. Principe, P. C. Maturan and L. Holongbayan for assistance with field management, tissue sampling and trait measurements; the staff of IRRI’s Climate Unit for providing weather data; Z. Fresquez for help with tissue processing; L. Harshman for assistance with a pilot RNA-seq run; the New York University Center for Genomics and Systems Biology GenCore Facility for sequencing support; and New York University High Performance Computing for supplying computational resources. We are grateful to current and former members of the Purugganan laboratory (particularly J. Flowers, R. Gutaker, A. Plessis, O. Wilkins and M. Zaidem) and the IRRI Strategic Innovation and Rice Breeding research platforms (particularly S. Dixit, A. Kohli, Y. Ludwig, K. McNally, R. Oliva, V. Roman-Reyna and N. Tsakirpaloglou) for insightful discussions; M. Quintana for sharing scripts in R; and S. Zaaijer for codesigning the figures. This work was funded in part by grants from the Zegar Family Foundation, the National Science Foundation Plant Genome Research Program and the NYU Abu Dhabi Research Institute to M.D.P., a fellowship from the Natural Sciences and Engineering Research Council of Canada through Grant PDF-502464-2017 to Z.J.-L., and a fellowship from the Gordon and Betty Moore Foundation/Life Sciences Research Foundation through Grant GBMF2550.06 to S.C.G.
Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature Limited.
Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.
PY - 2020/2/27
Y1 - 2020/2/27
N2 - Levels of gene expression underpin organismal phenotypes1,2, but the nature of selection that acts on gene expression and its role in adaptive evolution remain unknown1,2. Here we assayed gene expression in rice (Oryza sativa)3, and used phenotypic selection analysis to estimate the type and strength of selection on the levels of more than 15,000 transcripts4,5. Variation in most transcripts appears (nearly) neutral or under very weak stabilizing selection in wet paddy conditions (with median standardized selection differentials near zero), but selection is stronger under drought conditions. Overall, more transcripts are conditionally neutral (2.83%) than are antagonistically pleiotropic6 (0.04%), and transcripts that display lower levels of expression and stochastic noise7–9 and higher levels of plasticity9 are under stronger selection. Selection strength was further weakly negatively associated with levels of cis-regulation and network connectivity9. Our multivariate analysis suggests that selection acts on the expression of photosynthesis genes4,5, but that the efficacy of selection is genetically constrained under drought conditions10. Drought selected for earlier flowering11,12 and a higher expression of OsMADS18 (Os07g0605200), which encodes a MADS-box transcription factor and is a known regulator of early flowering13—marking this gene as a drought-escape gene11,12. The ability to estimate selection strengths provides insights into how selection can shape molecular traits at the core of gene action.
AB - Levels of gene expression underpin organismal phenotypes1,2, but the nature of selection that acts on gene expression and its role in adaptive evolution remain unknown1,2. Here we assayed gene expression in rice (Oryza sativa)3, and used phenotypic selection analysis to estimate the type and strength of selection on the levels of more than 15,000 transcripts4,5. Variation in most transcripts appears (nearly) neutral or under very weak stabilizing selection in wet paddy conditions (with median standardized selection differentials near zero), but selection is stronger under drought conditions. Overall, more transcripts are conditionally neutral (2.83%) than are antagonistically pleiotropic6 (0.04%), and transcripts that display lower levels of expression and stochastic noise7–9 and higher levels of plasticity9 are under stronger selection. Selection strength was further weakly negatively associated with levels of cis-regulation and network connectivity9. Our multivariate analysis suggests that selection acts on the expression of photosynthesis genes4,5, but that the efficacy of selection is genetically constrained under drought conditions10. Drought selected for earlier flowering11,12 and a higher expression of OsMADS18 (Os07g0605200), which encodes a MADS-box transcription factor and is a known regulator of early flowering13—marking this gene as a drought-escape gene11,12. The ability to estimate selection strengths provides insights into how selection can shape molecular traits at the core of gene action.
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U2 - 10.1038/s41586-020-1997-2
DO - 10.1038/s41586-020-1997-2
M3 - Article
C2 - 32051590
AN - SCOPUS:85079709979
VL - 578
SP - 572
EP - 576
JO - Nature Cell Biology
JF - Nature Cell Biology
SN - 1465-7392
IS - 7796
ER -