• This record comes from PubMed

MADS-box encoding gene Tunicate1 positively controls maize yield by increasing leaf number above the ear

. 2024 Nov 12 ; 15 (1) : 9799. [epub] 20241112

Language English Country England, Great Britain Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
2022YFF1003400 National Natural Science Foundation of China (National Science Foundation of China)

Links

PubMed 39532880
PubMed Central PMC11557842
DOI 10.1038/s41467-024-54148-7
PII: 10.1038/s41467-024-54148-7
Knihovny.cz E-resources

The leaves above the ear serve as a major source of carbohydrates for grain filling in maize. However, increasing the number of leaves above the ear to strengthen the source and improve maize yield remains challenging in modern maize breeding. Here, we clone the causative gene of the quantitative trait locus (QTL) associated with the number of leaves above the ear. The causative gene is the previously reported MADS-box domain-encoding gene Tunicate1 (Tu1), which is responsible for the phenotype of pod corn or Tunicate maize. We show that Tu1 can substantially increase the leaf number above the ear while maintaining the source‒sink balance. A distal upstream 5-base pair (bp) insertion of Tu1 originating from a popcorn landrace enhances its transcription, coregulates its plastochron activators and repressors, and increases the number of leaves above the ear. Field tests demonstrate that the 5-bp insertion of Tu1 can increase grain yields by 11.4% and 9.5% under regular and dense planting conditions, respectively. The discovery of this favorable Tu1 allele from landraces suggests that landraces represent a valuable resource for high-yield breeding of maize.

Erratum In

PubMed

See more in PubMed

Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. USA108, 20260–20264 (2011). PubMed PMC

Shaver, D. L. Genetics and breeding of maize with extra leaves above the ear. In Proceedings of 38th Annual Corn and Sorghum Research Conference (Chicago, IL: American Seed Trade Association), 161-180 (1983).

Stewart, D. W., Dwyer, L. M., Andrews, C. J. & Dugas, J. A. Modeling carbohydrate production, storage, and export in leafy and normal maize (Zea mays L.). Crop Sci. 37, 1228–1236 (1997).

Palmer, A., Heichel, G. H. & Musgrave, R. B. Patterns of translocation, respiratory loss, and redistribution of 14c in maize labeled after flowering. Crop Sci.13, 371–376 (1973).

Kaplan, D. R. Fundamental concepts of leaf morphology and morphogenesis: A contribution to the interpretation of molecular genetic mutants. Int. J. Plant Sci.162, 465–474 (2001).

Langdale, J. A. The then and now of maize leaf development. Maydica50, 459–467 (2005).

Colasanti, J. & Muszynski, M. The maize floral transition. Handbook of Maize Its Biology, 41-55 (2009).

Telfer, A., Bollman, K. M. & Poethig, R. S. Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development124, 645–654 (1997). PubMed

Vollbrecht, E., Veit, B., Sinha, N. & Hake, S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature350, 241–243 (1991). PubMed

Itoh, J. I., Hasegawa, A., Kitano, H. & Nagato, Y. A recessive heterochronic mutation, plastochron1, shortens the plastochron and elongates the vegetative phase in rice. Plant Cell10, 1511–1522 (1998). PubMed PMC

Miyoshi, K. et al. PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc. Natl. Acad. Sci. USA101, 875–880 (2004). PubMed PMC

Kawakatsu, T. et al. PLASTOCHRON2 regulates leaf initiation and maturation in rice. Plant Cell18, 612–625 (2006). PubMed PMC

Kawakatsu, T. et al. PLASTOCHRON3/GOLIATH encodes a glutamate carboxypeptidase required for proper development in rice. Plant J.58, 1028–1040 (2009). PubMed

Veit, B., Briggs, S. P., Schmidt, R. J., Yanofsky, M. F. & Hake, S. Regulation of leaf initiation by the terminal ear 1 gene of maize. Nature393, 166–168 (1998). PubMed

Wang, F. et al. ZmTE1 promotes plant height by regulating intercalary meristem formation and internode cell elongation in maize. Plant Biotechnol. J.20, 526–537 (2022). PubMed PMC

Suzuki, M. et al. The Maize Viviparous8 locus, encoding a putative ALTERED MERISTEM PROGRAM1-like peptidase, regulates abscisic acid accumulation and coordinates embryo and endosperm development. Plant Physiol.146, 1193–1206 (2008). PubMed PMC

Helliwell, C. A. et al. The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell13, 2115–2125 (2001). PubMed PMC

HARLAN, H. V. & POPE, M. N. Many-noded dwarf barley. J. Heredity13, 269–273 (1922).

Mascher, M. et al. Mapping-by-sequencing accelerates forward genetics in barley. Genome Biol.15, R78 (2014). PubMed PMC

Walla, A. et al. An Acyl-CoA N-Acyltransferase regulates meristem phase change and plant architecture in barley. Plant Physiol.183, 1088–1109 (2020). PubMed PMC

Hibara, K. I. et al. Regulation of the plastochron by three many-noded dwarf genes in barley. PLoS Genet17, e1009292 (2021). PubMed PMC

Chuck, G. S., Brown, P. J., Meeley, R. & Hake, S. Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proc. Natl Acad. Sci. USA111, 18775–18780 (2014). PubMed PMC

Suzuki, M., Sato, Y., Wu, S., Kang, B. H. & McCarty, D. R. Conserved functions of the MATE transporter BIG EMBRYO1 in Regulation of lateral organ size and initiation rate. Plant Cell27, 2288–2300 (2015). PubMed PMC

Alter, P. et al. Flowering time-regulated genes in maize include the transcription factor ZmMADS1. Plant Physiol.172, 389–404 (2016). PubMed PMC

Heuer, S. et al. The maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development, in egg cells, and early embryogenesis. Plant physiol.127, 33–45 (2001). PubMed PMC

Gallavotti, A. et al. The relationship between auxin transport and maize branching. Plant Physiol. 147, 1913–1923 (2008). PubMed PMC

Bommert, P. et al. thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development132, 1235–1245 (2005). PubMed

Wingen, L. U. et al. Molecular genetic basis of pod corn (Tunicate maize). Proc. Natl Acad. Sci. USA109, 7115–7120 (2012). PubMed PMC

Wang, J., Zhang X. & Lin Z. QTL mapping in a maize F2 population using genotyping-by-sequencing and a modified fine-mapping strategy. Plant Sci. 276, 171–180 (2018). PubMed

Han, J.-J., Jackson, D. & Martienssen, R. Pod corn is caused by rearrangement at the Tunicate1 locus. Plant Cell24, 2733–2744 (2012). PubMed PMC

Hartmann, U. et al. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J.21, 351–360 (2000). PubMed

Yu, J., Holland, J. B., McMullen, M. D. & Buckler, E. S. Genetic design and statistical power of nested association mapping in maize. Genetics178, 539–551 (2008). PubMed PMC

Buckler, E. S. et al. The genetic architecture of maize flowering time. Science325, 714–718 (2009). PubMed

Hufford, M. B. et al. De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science373, 655–662 (2021). PubMed PMC

Tian, T. et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122–W129 (2017). PubMed PMC

Satterlee, J. W. et al. A Wox3-patterning module organizes planar growth in grass leaves and ligules. Nat. Plants9, 720–732 (2023). PubMed PMC

Pollock, R. & Treisman, R. Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev.5, 2327–2341 (1991). PubMed

Shore, P. & Sharrocks, A. D. The MADS-box family of transcription factors. Eur. J. Biochem.229, 1–13 (1995). PubMed

Li, D. et al. The genetic architecture of leaf number and its genetic relationship to flowering time in maize. N. Phytol.210, 256–268 (2016). PubMed PMC

Ng, M. & Yanofsky, M. F. Function and evolution of the plant MADS-box gene family. Nat. Rev. Genet.2, 186–195 (2001). PubMed

Gregis, V. et al. Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis. Genome Biol.14, R56 (2013). PubMed PMC

Hufford, M. B. et al. Comparative population genomics of maize domestication and improvement. Nat. Genet.44, 808–811 (2012). PubMed PMC

Broman, K. W., Hao, W., Śaunak, S. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics, 19, 889–890 (2003). PubMed

Vega, J. M., Yu, W., Kennon, A. R., Chen, X. & Zhang, Z. J. Improvement of agrobacterium-mediated transformation in Hi-II maize (Zea mays) using standard binary vectors. Plant Cell Rep.27, 297–305 (2008). PubMed

Bradbury, P. J., Zhang, Z., Kroon, D. E., Casstevens, T. M. & Buckler, E. S. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics23, 2633–2635 (2007). PubMed

Zhang, X. et al. The tin1 gene retains the function of promoting tillering in maize. Nat. Commun.10, 5608 (2019). PubMed PMC

Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics30, 2114–2120 (2014). PubMed PMC

Mi, Z., Sun, H., Fei, Z., Feng, Z. & Shan, G. Fastq_clean: An optimized pipeline to clean the Illumina sequencing data with quality control. 2014 IEEE International Conference on Bioinformatics and Biomedicine (BIBM). 2015.

Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics29, 15–21 (2013). PubMed PMC

Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc.7, 562–578 (2012). PubMed PMC

Bartlett, A. et al. Mapping genome-wide transcription-factor binding sites using DAP-seq. Nat. Protoc.12, 1659–1672 (2017). PubMed PMC

O’Malley, R. C. et al. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell165, 1280–1292 (2016). PubMed PMC

Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics34, i884–i890 (2018). PubMed PMC

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods9, 357–359 (2012). PubMed PMC

Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics25, 2078–2079 (2009). PubMed PMC

Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol.9, R137 (2008). PubMed PMC

Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res.37, W202–W208 (2009). PubMed PMC

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods25, 402 (2001). PubMed

Librado, P. & Rozas, J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics25, 1451–1452 (2009). PubMed

See more in PubMed

BioProject
PRJNA960713

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...