Rewiring Gene Circuitry for Plant Improvement

Overview

Journal Nat Genet

Specialty Genetics

Date 2024 Jul 29

PMID 39075207

Authors

Alexander T Borowsky

Julia Bailey-Serres

Affiliations

Soon will be listed here.

Abstract

Aspirations for high crop growth and yield, nutritional quality and bioproduction of materials are challenged by climate change and limited adoption of new technologies. Here, we review recent advances in approaches to profile and model gene regulatory activity over developmental and response time in specific cells, which have revealed the basis of variation in plant phenotypes: both redeployment of key regulators to new contexts and their repurposing to control different slates of genes. New synthetic biology tools allow tunable, spatiotemporal regulation of transgenes, while recent gene-editing technologies enable manipulation of the regulation of native genes. Ultimately, understanding how gene circuitry is wired to control form and function across varied plant species, combined with advanced technology to rewire that circuitry, will unlock solutions to our greatest challenges in agriculture, energy and the environment.

Citing Articles

Evolutionary innovation hints at ways to engineer efficient photosynthesis in crops.

Rath M, Bergmann D Nature. 2024; 636(8041):53-54.

PMID: 39567797 DOI: 10.1038/d41586-024-03553-5.

A novel interpretable deep learning-based computational framework designed synthetic enhancers with broad cross-species activity.

Li Z, Zhang Y, Peng B, Qin S, Zhang Q, Chen Y Nucleic Acids Res. 2024; 52(21):13447-13468.

PMID: 39420601 PMC: 11602155. DOI: 10.1093/nar/gkae912.

References

Lobell D, Schlenker W, Costa-Roberts J . Climate trends and global crop production since 1980. Science. 2011; 333(6042):616-20. DOI: 10.1126/science.1204531. View

Bailey-Serres J, Parker J, Ainsworth E, Oldroyd G, Schroeder J . Genetic strategies for improving crop yields. Nature. 2019; 575(7781):109-118. PMC: 7024682. DOI: 10.1038/s41586-019-1679-0. View

Mueller N, Gerber J, Johnston M, Ray D, Ramankutty N, Foley J . Closing yield gaps through nutrient and water management. Nature. 2012; 490(7419):254-7. DOI: 10.1038/nature11420. View

Mickelbart M, Hasegawa P, Bailey-Serres J . Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet. 2015; 16(4):237-51. DOI: 10.1038/nrg3901. View

Jez J, Lee S, Sherp A . The next green movement: Plant biology for the environment and sustainability. Science. 2016; 353(6305):1241-4. DOI: 10.1126/science.aag1698. View

Meng F, Zhao H, Zhu B, Zhang T, Yang M, Li Y . Genomic editing of intronic enhancers unveils their role in fine-tuning tissue-specific gene expression in Arabidopsis thaliana. Plant Cell. 2021; 33(6):1997-2014. PMC: 8290289. DOI: 10.1093/plcell/koab093. View

Reyna-Llorens I, Burgess S, Reeves G, Singh P, Stevenson S, Williams B . Ancient duons may underpin spatial patterning of gene expression in C leaves. Proc Natl Acad Sci U S A. 2018; 115(8):1931-1936. PMC: 5828626. DOI: 10.1073/pnas.1720576115. View

Weirauch M, Yang A, Albu M, Cote A, Montenegro-Montero A, Drewe P . Determination and inference of eukaryotic transcription factor sequence specificity. Cell. 2014; 158(6):1431-1443. PMC: 4163041. DOI: 10.1016/j.cell.2014.08.009. View

OMalley R, Huang S, Song L, Lewsey M, Bartlett A, Nery J . Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape. Cell. 2016; 165(5):1280-1292. PMC: 4907330. DOI: 10.1016/j.cell.2016.04.038. View

10.

Lambert S, Yang A, Sasse A, Cowley G, Albu M, Caddick M . Similarity regression predicts evolution of transcription factor sequence specificity. Nat Genet. 2019; 51(6):981-989. DOI: 10.1038/s41588-019-0411-1. View

11.

Rhoades M, Reinhart B, Lim L, Burge C, Bartel B, Bartel D . Prediction of plant microRNA targets. Cell. 2002; 110(4):513-20. DOI: 10.1016/s0092-8674(02)00863-2. View

12.

Hayden C, Jorgensen R . Identification of novel conserved peptide uORF homology groups in Arabidopsis and rice reveals ancient eukaryotic origin of select groups and preferential association with transcription factor-encoding genes. BMC Biol. 2007; 5:32. PMC: 2075485. DOI: 10.1186/1741-7007-5-32. View

13.

van der Horst S, Filipovska T, Hanson J, Smeekens S . Metabolite Control of Translation by Conserved Peptide uORFs: The Ribosome as a Metabolite Multisensor. Plant Physiol. 2019; 182(1):110-122. PMC: 6945846. DOI: 10.1104/pp.19.00940. View

14.

Nolan T, Shahan R . Resolving plant development in space and time with single-cell genomics. Curr Opin Plant Biol. 2023; 76:102444. DOI: 10.1016/j.pbi.2023.102444. View

15.

Gaudinier A, Brady S . Mapping Transcriptional Networks in Plants: Data-Driven Discovery of Novel Biological Mechanisms. Annu Rev Plant Biol. 2016; 67:575-94. DOI: 10.1146/annurev-arplant-043015-112205. View

16.

Li M, Yao T, Lin W, Hinckley W, Galli M, Muchero W . Double DAP-seq uncovered synergistic DNA binding of interacting bZIP transcription factors. Nat Commun. 2023; 14(1):2600. PMC: 10163045. DOI: 10.1038/s41467-023-38096-2. View

17.

Pratapa A, Jalihal A, Law J, Bharadwaj A, Murali T . Benchmarking algorithms for gene regulatory network inference from single-cell transcriptomic data. Nat Methods. 2020; 17(2):147-154. PMC: 7098173. DOI: 10.1038/s41592-019-0690-6. View

18.

Cirrone J, Brooks M, Bonneau R, Coruzzi G, Shasha D . OutPredict: multiple datasets can improve prediction of expression and inference of causality. Sci Rep. 2020; 10(1):6804. PMC: 7176633. DOI: 10.1038/s41598-020-63347-3. View

19.

Buenrostro J, Giresi P, Zaba L, Chang H, Greenleaf W . Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods. 2013; 10(12):1213-8. PMC: 3959825. DOI: 10.1038/nmeth.2688. View

20.

Marand A, Schmitz R . Single-cell analysis of cis-regulatory elements. Curr Opin Plant Biol. 2021; 65:102094. DOI: 10.1016/j.pbi.2021.102094. View