Defects in meristem maintenance, cell division, and cytokinin signaling are early responses in the boron deficient maize mutant tassel-less1

Authors: MATTHES, MICHAELA - University Of Bonn; DARNELL, ZOE - University Of Missouri; Best, Norman; GUTHRIE, KATY - University Of Missouri; ROBIL, JANLO - University Of Missouri; AMSTUTZ, JEN - University Of Missouri; DURBAK, AMANDA - University Of Missouri; MCSTEEN, PAULA - University Of Missouri

Submitted to: Physiologia Plantarum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2022
Publication Date: 3/16/2022
Citation: Matthes, M.S., Darnell, Z., Best, N.B., Guthrie, K., Robil, J.M., Amstutz, J., Durbak, A., McSteen, P. 2022. Defects in meristem maintenance, cell division, and cytokinin signaling are early responses in the boron deficient maize mutant tassel-less1. Physiologia Plantarum. 174(2): Article e13670. https://doi.org/10.1111/ppl.13670.
DOI: https://doi.org/10.1111/ppl.13670

Interpretive Summary: The basic tenet of biology is that phenotypes are shaped by both the genetic makeup and the environment. Therefore, understanding how environmental and genetic factors integrate is a central question in developmental biology. Many of the advances in the field have been in understanding how root architecture is influenced by availability of nutrients, however less research has addressed the role of nutrients in development of above ground organs. The essential micronutrient boron has long been known to cause growth defects – farmers describe it as “the growing tip stops growing” – but a full mechanistic understanding of how limited boron supply leads to growth defects is lacking. In plants, deficiencies of the micronutrient boron cause growth defects especially in meristems, groups of stem cells, from which all organs develop. This study indicates direct functional involvement of boron in specific meristem maintenance pathways in maize by regulation of the the gene, knotted1, exemplifying how genetic and environmental factors integrate during meristem development and explaining why meristematic tissues are particularly affected under boron limitation. Knowledge about how nutrient availability integrates into meristem development is agriculturally important, since nutrient deficiencies often lead to a general growth arrest and can severely reduce crop yield.

Technical Abstract: Meristems house the stem cells needed for the developmental plasticity observed in adverse environmental conditions and are crucial for determining plant architecture. Meristem development is particularly sensitive to deficiencies of the micronutrient boron, yet how boron integrates into meristem development pathways is unknown. We addressed this question using the boron-deficient maize mutant, tassel-less1 (tls1). Reduced boron uptake in tls1 leads to a progressive impairment of meristem development that manifests in vegetative and reproductive defects. We show, that the tls1 tassel phenotype (male reproductive structure) was partially suppressed by mutations in the CLAVATA1 (CLV1)-ortholog, thick tassel dwarf1 (td1), but not by other mutants in the well characterized CLV-WUSCHEL pathway, which controls meristem size. The suppression of tls1 by td1 correlates with altered signaling of the phytohormone cytokinin. In contrast, mutations in the meristem maintenance gene knotted1 (kn1) enhanced both vegetative and reproductive defects in tls1. In addition, reduced transcript levels of kn1 and cell cycle genes are early defects in tls1 tassel meristems. Our results show that specific meristem maintenance and hormone pathways are affected in tls1, and suggest that reduced boron levels induced by tls1 are the underlying cause of the observed defects. We, therefore, provide new insights into the molecular mechanisms affected by boron deficiency in maize, leading to a better understanding of how genetic and environmental factors integrate during shoot meristem development.