Dissecting the TOR–S6K signal transduction pathway in maize seedlings: relevance on cell growth regulation

Abstract

Insulin and ‘insulin‐like’ growth factors (IGFs) are known to regulate cell growth in eukaryotes by stimulating a signal transduction pathway that exerts translational control. Intermediate kinases of this pathway, target of rapamycin (TOR) and ribosomal protein S6 kinase (S6K), have been reported in Arabidospsis thaliana and Zea mays. However, upstream signal inducers and downstream targets of the pathway are not well known in plants. The objective of this work is to inquire whether plant growth is regulated by a signal transduction pathway similar to the insulin/IGF‐stimulated pathway in other metazoans. Insulin as well as Zea mays insulin‐related peptide (ZmIGF), which is a maize, 20‐kDa peptide fraction recognized by insulin antibody, were used as effectors to stimulate maize axes growth from germinating seeds. ZmIGF expression was identified in axes from germinating maize seeds and immunolocalized in the meristems of these tissues. Significant enhancement of specific de novo protein synthesis of the translational apparatus components was found in the stimulated axes. Reverse‐transcription‐polymerase chain reaction analysis of total and polysomal RNA pools in ZmIGF‐ or insulin‐stimulated axes confirmed these data by revealing specific mRNA recruitment into polysomes. In addition, the same stimuli induced activation of S6 ribosomal protein kinase (ZmS6K) in germinating maize axes. All the above effects were inhibited by rapamycin, indicating that they depend on TOR activity. We conclude that a TOR–S6K signal transduction pathway is functional in maize germination, as that found for non‐photosynthetic eukaryotes. The evolutionary implications of these findings are discussed.

Coordination of cell growth and cell division in maize (Zea mays L.) relevance of the conserved TOR signal transduction pathway

“…This study confirms and extends previous work (Dinkova et al 2007) by demonstrating that insulin or the maize growth factor ZmIGF signal input is capable of regulating cell growth and cell division in maize tissues, similarly as reported for insulin or IGFs in nonphotosynthetic eukaryotic cells (Averous and Proud 2006). Coordination of these two major events has been reported as a universal need to maintain cell size homeostasis in many different biological systems (Jorgensen and Tyers 2004;Holtz et al 2005).…”

“…4B). In support of this interpretation, previous reports have demonstrated functional TOR and S6K kinases in maize (Reyes-de la Cruz et al 2004;Agredano-Moreno et al 2007), which also demonstrate sensitivity to rapamycin inhibition (Dinkova et al 2007).…”

“…Interestingly, insulin is capable of stimulating PI3K-TOR pathway in maize tissues, and it significantly speeds up maize germination and seedling growth, similar to a maize peptide (ZmIGF), recognized by insulin antibody present in embryonic axes or maize calluses (García-Flores et al 2001). In both cases, these effects were inhibited by rapamycin (Dinkova et al 2007). Based on these antecedents, the purpose of this research is to extend our knowledge of the role of the PI3K-TOR pathway in plants, by inquiring about the essential targets that contribute to coordinate the regulation of cell growth and cell division in maize.…”

Plant TOR signaling components

“…The time of IGF expression coincides with the onset of fast growth during germination. 30 When maize seeds were treated with isolated IGF, a significant increment in coleoptile and root …”

The TOR Pathway Modulates the Structure of Cell Walls inArabidopsis

“…Ncs6p, together with other proteins, has been shown to transfer the sulfur group during 2-thiouridine formation (Bjö rk et al, 2007;Schlieker et al, 2008;Leidel et al, 2009;Noma et al, 2009). The TOR pathway is involved in regulating the translational machinery in different organisms, including plants (Mahfouz et al, 2006;Wullschleger et al, 2006;Dinkova et al, 2007), and the lack of tRNA modifications might trigger signals that feed back into TOR signaling. This indirect effect on the TOR pathway is a possible explanation for the rapamycin hypersensitivity of the Dncs6 mutant (Chan et al, 2000;Goehring et al, 2003a).…”