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ARS Home » Pacific West Area » Albany, California » Plant Gene Expression Center » Research » Publications at this Location » Publication #408763
Research Project: Developmental and Environmental Control Mechanisms to Enhance Plant Productivity

Location: Plant Gene Expression Center

Title: A regulatory network controlling developmental boundaries and meristem fates contributed to maize domestication

Author
item DONG, ZHAOBIN - University Of California Berkeley
item HU, GAOYUAN - China Agricultural University
item CHEN, QIUYUE - University Of California Berkeley
item SHEMYAKINA, ELENA - University Of California Berkeley
item CHAU, GEEYUN - University Of California Berkeley
item WHIPPLE, CLINTON - Brigham Young University
item Fletcher, Jennifer
item CHUCK, GEORGE - University Of California Berkeley

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/9/2024
Publication Date: 10/16/2024
Citation: Dong, Z., Hu, G., Chen, Q., Shemyakina, E.A., Chau, G., Whipple, C., Fletcher, J.C., Chuck, G. 2024. A regulatory network controlling developmental boundaries and meristem fates contributed to maize domestication. Nature Genetics. 56:2528–2537. https://doi.org/10.1038/s41588-024-01943-z.
DOI: https://doi.org/10.1038/s41588-024-01943-z

Interpretive Summary: Epistasis, the process by which different loci genetically interact, is very often a confounding factor when identifying domestication loci.  For example, when association analysis is used to identify these loci, epistasis can mask the effects of one domestication gene on another.  Thus, if several domestication loci are part of an epistatic gene network, their interactions may be hidden, and impede the identification of new genes. In our manuscript, we bypass the epistasis problem by starting with the cloned genes, and then identify downstream and upstream direct interactions using a combination of chromatin immunoprecipitation sequencing, genome wide association analysis, joint linkage mapping and higher order genetic and expression analysis.  Using all these tools together, we identify a new domestication transcription factor, tasselsheath4, that acts directly upstream of several classical maize domestication loci such as teosinte branched1, tassels replace upper ears1 and teosinte glume architecture1.  We show that tsh4 controls key traits selected by early farmers including repression of tillering, control of axillary branch sexuality, as well as increased kernel weight.  Moreover, by uncovering all the direct targets of tsh4, we discovered a novel mechanism of function that has yet to be described in plants.  The tsh4 transcript is negatively regulated by the MIR529 and MIR156 microRNAs, but TSH4 also binds to, and represses the expression of these same microRNAs in a double negative feedback loop.  Using simultaneous MIR529 microRNA in situ hybridization and TSH4 immunolocalization, we show how this mutual negative autoregulatory mechanism establishes a very tight boundary between meristem and lateral organs.  We demonstrate that this boundary is necessary for the development of the two kerneled spikelet pair, a structure responsible for the doubling of seed yield in domesticated maize compared to its teosinte ancestor that only has single kernel spikelets.  meristem.  These combined data places tsh4 at the very top of the maize domestication hierarchy, and gives us a clearer understanding of how ancient farmers were able to transform a simple weed into an essential crop plant we depend on today.

Technical Abstract: Early farmers selected for different sets of vegetative and reproductive traits during domestication, but identifying the causative loci has been hampered by their epistasis and functional redundancy.  Using ChIP-seq combined with genome wide association analysis, we uncovered a developmental regulator that controls both categories of traits while acting upstream of multiple domestication loci.   tasselsheath4 is a new maize domestication gene establishes developmental boundaries and specifies meristem fates despite not being expressed in meristems.   TSH4 does this by employing an unusual mechanism where it targets and represses the very same microRNAs that negatively regulate it via a double negative feedback loop.  tasselsheath4 functions redundantly with a pair of homologs to positively regulate a suite of domestication loci and specify the meristem that doubled seed yield in modern maize.  Thus, tasselsheath4 played a critical role in yield gain and helped generate ideal crop plant architecture, thus explaining why it was a major domestication target.