Our laboratory used genetics to study plant development. Using mutants with interesting developmental phenotypes, we were able to identify genes that control plant architecture and determine their mechanism of action. Because plant architecture results from activities of meristems, our lab often discovered genes that regulate meristem activity. The mutants were discovered using the rich resources of maize genetics. The first mutant identified was Knotted1, a homeobox gene that is normally only expressed in meristems and not leaves. The dominant mutant has interesting leaf form due to misexpression of the Knotted1 gene in the leaf. This mutant led us to think about the boundary between the blade and the sheath of the leaf. With other mutants, we discovered that the genes that create this boundary also function at the boundary of other organs, such as tassel branches.
Some mutants only affected the inflorescence, such as Tasselseed5, which made the normally male apical inflorescence female. Others were pleiotropic with defects in leaf and inflorescence development.
The role of knox genes in maize and other species
Knotted1-like homeobox (knox) genes are expressed in meristems and are specifically down-regulated as leaf primordia initiate. Dominant mutants exist in maize that misexpress knox genes in leaves, leading to striking proximal-distal defects. Recessive knox mutants in maize, rice and Arabidopsis fail to elaborate a shoot, thus revealing a function for knox genes in the meristem. We identified the targets of KNOTTED1 in maize and carried out similar experiments in rice. Most of the hormone pathways are regulated by KN1.
A dominant Knotted1 mutant that results from a transposon insertion in the intron. The normally smooth leaves have bumps (knots) that result from blade cells adopting sheath fate.
Inflorescence architecture in maize and other grasses
Nearly all grasses are characterized by the spikelet, a short branch that contains floral meristems. The diversity in the grasses reflects variation in the organization of spikelets that ultimately originates from activities of meristems. With NSF support, we identified many of the genes that regulate inflorescence architecture in maize. These genes are defined by their mutant phenotypes.
A scanning electron micrograph of an ear primordia showing rows of spikelet meristems, each of which will develop into a kernel.
Positional signaling in maize leaf development
The maize leaf offers a unique opportunity to study how cells respond to their position and differentiate accordingly. The proximal part of the maize leaf is the sheath, a tissue that wraps around the culm. The distal part of the leaf is the blade, which lays flat to optimize photosynthesis. At the junction of the sheath and blade is the ligule region. In addition to this major proximal-distal axis, the abaxial-adaxial and medial-lateral axes are also defined by distinct cell types and tissue organization. How these axes are established and coordinated is not known. We used maize mutants to identify the genes that regulate this coordinate system.
The front (abaxial surface) and back (adaxial surface) of a maize leaf.
Y. Du, C. Lunde,Y. Li, D. Jackson, S. Hake, Z. Zhang. 2021. Gene duplication at the Fascicled ear1 locus controls the fate of inflorescence meristem cells in maize. 118(7) e2019218118.
Kraemer, F.J., Lunde, C., Koch, M., Kuhn, B.M., Ruehl, C., Brown, P.J., Hoffmann, P., Göhre, V., Hake, S., Pauly, M. and Ramírez, V., 2021. A mixed-linkage (1, 3; 1, 4)-β-D-glucan specific hydrolase mediates dark-triggered degradation of this plant cell wall polysaccharide. Plant Physiology, 185(4), pp.1559-1573.
Lunde C, Kimberlin A, Leiboff S, Koo AJ, Hake S. (2019) Tasselseed5 overexpresses a wound-inducible enzyme, ZmCYP94B1, that affects jasmonate catabolism, sex determination and plant architecture in maize. Commun Biol. Mar 25;2:114. doi: 10.1038/s42003-019-0354-1.
Anderson, A.A., Aubin, B.S., Abraham-Juarez, M.J., Leiboff, S., Shen, Z., Briggs, S.P., Brunkard, J.O., Hake, S., 2019. The second site modifier, Sympathy for the ligule, encodes a homolog of Arabidopsis ENHANCED DISEASE RESISTANCE4 and rescues the liguleless narrow maize mutant. The Plant Cell. 31(8):1829-1844
Leiboff, S. and Hake, S. 2019. Reconstructing the transcriptional ontogeny of maize and sorghum supports an inverse hourglass model of inflorescence development. Current Biology. 29(20):3410-3419.
Zhang D, Sun W, Singh R, Zheng Y, Cao Z, Li M, Lunde C, Hake S, Zhang Z. (2018) GRF-interacting factor1 Regulates Shoot Architecture and Meristem Determinacy in Maize. Plant Cell. 30(2):360-374.
Tsuda, K, Abraham-Juarez, MJ, Maeno, A, Dong, Z, Aromdee, D, Meeley, R, Shiroishi, T, Nonomura, K and Hake, S. (2017) KNOTTED1 cofactors, BLH12 and BLH14, regulate internode patterning and vein anastomosis in maize. Plant Cell. 29(5):1105-1118.
Rosa M, Abraham-Juarez MJ, Lewis MW, Fonseca JP, Tian W, Ramirez V, Luan S, Pauly M, Hake S. (2017) The Maize MID-COMPLEMENTING ACTIVITY Homolog CELL NUMBER REGULATOR13/NARROW ODD DWARF Coordinates Organ Growth and Tissue Patterning. Plant Cell 29(3):474-490.
Tsuda, K. Kurata, N. Ohyanagi, H. and Hake, S. (2014) Genome-Wide Study of KNOX Regulatory Network Reveals Brassinosteroid Catabolic Genes Important for Shoot Meristem Function in Rice. Plant Cell 26:3488-500.
Thompson BE, Basham C, Hammond R, Ding Q, Kakrana A, Lee TF, Simon SA, Meeley, R, Meyers, BC and Hake, S. (2014) The dicerlike-1 homologue, fuzzy tassel, is required for the regulation of meristem determinacy in the inflorescence and vegetative growth in maize. Plant Cell 26:4702-17.
Lewis MW, Bolduc N, Hake K, Htike Y, Hay A, Candela H, Hake S. (2014) Gene regulatory interactions at lateral organ boundaries in maize. Development 141:4590-7.
Johnston, R, Wang, M., Sun, Q., Sylvester, A. W. Hake, S. and Scanlon, M. (2014) Transcriptomic analyses indicate that maize ligule development recapitulates gene expression patterns that occur during lateral organ initiation. Plant Cell 26:4718-4732
Chuck, G., Brown, P., Meeley, R., Hake, S. (2014) Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. PNAS 111: 18775-80.
Eveland, Andrea L. Goldshmidt, Alexander, Pautler,Michael, Hake, Sarah et al. Regulatory modules controlling maize inflorescence architecture. Genome Research December 4, 2013.
Bolduc, N. Tyers, R. Freeling, M. Hake, S. (2014) Unequal redundancies in KNOX genes. Plant Physiology 164: 229-38
O'Connor, D. L., Runions, A., Sluis, A., Bragg, J., Vogel, J. Prusinkiewicz, P. Hake, S. A Division in PIN-Mediated Auxin Patterning During Organ Initiation in Grasses (2014) Plos Computational Biology Jan 30, 2014.
Moon, J. Candela, H. and Hake, S. 2013. The Liguleless narrow mutation affects proximal-distal signaling and leaf growth. Development 140: 405-412.
Bolduc, N., Yilmaz, A., Mejia-Guerra, M.K., Morohashi, K., O'Connor, D., Grotewold, E., and Hake, S. 2012. Unraveling the KNOTTED1 regulatory network in maize meristems Genes & Development 26: 1685-1690.
Chuck, G., Tobias, C., Sun, L., Kraemer, F., Li, C., Dibble, D., Arora, R., Bragg, J. N., Vogel, J. P., Singh, S., Simmons, B., Pauly, M., Hake, S. (2011) Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility and increases starch content of switchgrass PNAS 108:17550-17555.
Chuck, G. Whipple, C., Jackson, D. and Hake, S. (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and establishment of meristem boundaries. Development 137:1243-1250
Ramirez, J. Bolduc, N., Lisch, D., and Hake, S. (2009) Distal expression of knotted1 in maize leaves leads to re-establishment of proximal/distal patterning and leaf dissection. Plant Physiology 151:1878-88.
Thompson, B., Bartling, L., Whipple, C., Hall, D. Schmidt, R, and Hake, S. (2009) bearded-ear encodes a MADS-box transcription factor that controls floral meristem identity and determinacy in maize. Plant Cell 21:2578-90.
Bolduc, N. and Hake, S. (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21:1647-58.
Chuck G, Meeley R, Hake S. (2008) Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1. Development 135:3013-9.
Magnani, E. and Hake, S. (2008) KNOX lost the OX: The Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 20: 875-887.
Chuck, G. Meeley, R. Irish, E., Sakai, H. Hake, S. (2007) The tasselseed4 microRNA of maize controls meristem cell fate and sex determination by targeting the indeterminate spikelet1/Tasselseed6 gene. Nature Genetics 12:1517-1521 PDF 448k
Chuck, G, Cigan, M., Saeteurn, K. Hake, S. (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nature Genetics, 39:544-549. PDF 448k
Bortiri, E., Chuck, G., Vollbrecht, E., Rocheford, T., Martienssen, R., Hake, S. ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell. 2006 Mar;18(3):574-85. PDF 448k
Member - ARS Hall of Science - 2013
ARS Senior Scientist of the Year - 2011
Fellow - American Association for the Advancement of Science - 2009
Member - National Academy of Sciences - 2009
Stephen Hales Prize - American Society of Plant Biology - 2008
Jeanette Siron Pelton Award - Botanical Society of America - 1996