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

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.

Cytokinins as boron deficiency signals to sustain shoot development in boron‐efficient oilseed rape

“…The fact that the CK forms with a high affinity to shoot CK receptors accumulated exclusively in the B-efficient accession, while the less active form DZR and the deactivated species CZROG and TZOG accumulated in the B-inefficient accession, points to a shoot growth-regulating role of these CK species, especially under low B. This conclusion is in line with the recent finding that CK signaling regulates early responses of B deficiency in maize, where a B-dependent CK signaling was shown to be important to prevent the progressive impairment of meristem development revealed by vegetative and reproductive defects (Matthes et al, 2022). Moreover, overexpression of a CK oxidase in maize roots, which leads to reduced CK levels, was shown to influence the shoot content of various nutrients (Ramireddy et al, 2021).…”

Exposure to boron trioxide nanoparticles and ions cause oxidative stress, DNA damage, and phenotypic alterations in Drosophila melanogaster as an in vivo model

“…Ince et al (2018) determined that the in vivo effects of boron on mRNA expression of OCT‐3/4, NANOG, and HEX genes in embryo and histological changes along fetal development. Matthes et al (2022) found that meristem maintenance, cytokinin signaling, and cell division as a result of boron insufficiency in maize mutant, tassel‐less1 (tls1).…”

“…Lastly, boron may have the potential to act in specific genes, domains, homeoproteins (as homeobox domain products), or transcription factors Ince et al (2018). determined that the in vivo effects of boron on mRNA expression of OCT-3/4, NANOG, and HEX genes in embryo and histological changes along fetal development Matthes et al (2022). found that meristem maintenance, cytokinin signaling, and cell division as a result of boron insufficiency in maize mutant, tassel-less1 (tls1).5 | CONCLUSIONOverall, our study showed that both B 2 O 3 NPs and its ionic form could exert certain detrimental effects on D. melanogaster at relatively high exposure doses, which highlights the significance of thorough examination and risk assessment of B 2 O 3 NPs for the first time.…”

Single‐cell transcriptomic analysis of pea shoot development and cell‐type‐specific responses to boron deficiency

“…One clear phenotype of B deficiency is the inhibition of root elongation (Poza-Viejo et al, 2018). Previous studies have shown that B deficiency affects normal physiological activities in the shoot, including impaired photosynthesis in MC (Figure 4d) (Han et al, 2008), impeding nutrient absorption and transport by affecting the stability of vascular bundles (Pommerrenig et al, 2019), and restricting the development of root meristem (Matthes et al, 2022). However, observing the effects of B deficiency on different cell types in the shoot apex at the single-cell transcript level is a novel aspect of this study.…”

“…Research has shown that meristem development is particularly sensitive to B deficiency (Poza‐Viejo et al., 2018). The reduced‐B‐uptake mutant tassel‐less1 ( tls1 ) in Z. mays exhibits defective SAM structure due to transcriptional repression of the meristem maintenance gene KN1 and cell cycle genes (Matthes et al., 2022). However, how B deficiency affects the regulation of meristem development and the key TFs involved in this process have yet to be discovered.…”