TOP1α fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars

Tang

Plant Signaling & Behavior

et al. 2022

Self Cite

Root gravitropism is important for anchorage and exploration of soil for water and nutrients. It affects root architecture, which is one of the elements that influence crop yield. The mechanism of primary root gravitropism has been widely studied, but it is still not clear how lateral root gravitropism is regulated. Here, in this study, we found that Topoisomerase I α (TOP1α) repressed lateral root gravitropic growth, which was opposite to the previous report that TOP1α maintains primary root gravitropism, revealing a dual function of TOP1α in root gravitropism regulation. Further investigation showed that Target of Rapamycin (TOR) was suppressed in columella cells of lateral root to inhibit columella cell development, especially amyloplast biosynthesis. Our findings uncovered a new mechanism about lateral root gravitropism regulation, which might provide a theoretical support for improving agricultural production.

Section: Discussionmentioning

confidence: 74%

“… 8 , 9 We found that TOP1α inhibits Target of Rapamycin (TOR) expression so that CCs are relatively stable to keep gravitropism, while other root cell division is promoted (like cells in meristem zone) when sucrose is produced through photosynthesis. 10 …”

Section: Introductionmentioning

confidence: 99%

TOP1α suppresses lateral root gravitropism in Arabidopsis

Tang

Plant Signaling & Behavior

et al. 2022

Self Cite

“…In response to photosynthesis-derived sugars, TOR phosphorylates E2 PROMOTER BINDING FACTOR (E2F) A in the RAM and promotes their activity in upregulating S-phase genes necessary for cell division (Xiong et al 2013 ). TOR has recently been shown to be required to maintain root tip homeostasis in response to photosynthesis-derived sugars during the heterotrophic-to-autotrophic transition, likely through regulation of PLETHORA2 (PLT2) and PIN2 stability (Zhang et al 2022 ). Furthermore, sugar-stimulated TOR activity in the root suppresses autophagy and maintains RAM activity to support root growth under nutrient-limiting conditions (Dong et al 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Regulation of early seedling establishment and root development in Arabidopsis thaliana by light and carbohydrates

Pasternak,

Kircher,

Palme

et al. 2023

Planta

Main conclusion Root development is regulated by sucrose and light during early seedling establishment through changes in the auxin response and chromatin topology. Abstract Light is a key environmental signal that regulates plant growth and development. The impact of light on development is primarily analyzed in the above-ground tissues, but little is known about the mechanisms by which light shapes the architecture of underground roots. Our study shows that carbohydrate starvation during skotomorphogenesis is accompanied by compaction of nuclei in the root apical meristem, which prevents cell cycle progression and leads to irreversible root differentiation in the absence of external carbohydrates, as evidenced by the lack of DNA replication and increased numbers of nuclei with specific chromatin characteristics. In these conditions, induction of photomorphogenesis was unable to restore seedling growth, as overall root growth was compromised. The addition of carbohydrates, either locally or systemically by transferring seedlings to sugar-containing medium, led to the induction of adventitious root formation with rapid recovery of seedling growth. Conversely, transferring in vitro carbohydrate-grown seedlings from light to dark transiently promoted cell elongation and significantly reduced root meristem size, but did not primarily affect cell cycle kinetics. We show that, in the presence of sucrose, dark incubation does not affect zonation in the root apical meristem but leads to shortening of the proliferative and transition zones. Sugar starvation led to a rapid increase in lysine demethylation of histone H3 at position K9, which preceded a rapid decline in cell cycle activity and activation of cell differentiation. In conclusion, carbohydrates are required for cell cycle activity, epigenetics reprogramming and for postmitotic cell elongation and auxin-regulated response in the root apical meristem.

“…Notably, the expression of PLT1 is still detected in the SCN in mto2-2 roots, indicating that the novel Thr pathway we report here is apparently independent of the PLT pathway. A remaining challenge will be to uncover how these pathways are interrelated, as the metabolic state has been shown to influence the stability of PLT2 ( Zhang et al, 2022 ). Experimental and computational approaches implemented here will be fundamental to uncover how the metabolic state regulates SC activity.…”

Section: Discussionmentioning

confidence: 99%

A mutation in THREONINE SYNTHASE 1 uncouples proliferation and transition domains of the root apical meristem: experimental evidence and in silico proposed mechanism

et al. 2022

A continuum from stem to transit-amplifying and to a differentiated cell state is a common theme in multicellular organisms. In the plant root apical meristem (RAM), transit-amplifying cells are organized in two domains, the proliferation domain (PD) from which the cells are displaced to the transition domain (TD), suggesting that both domains are necessarily coupled. Here we show that in a mutant, affected in threonine (Thr) synthesis (methionine overexpressor2-2), the RAM lacks the PD. Through a combination of cell length profile analysis, mathematical modeling, and molecular markers we establish that the PD and TD can be uncoupled. Remarkably, although the RAM of mto2-2 is represented solely by the TD, the known factors of RAM maintenance and auxin signaling are expressed in the mutant. Mathematical modelling predicts that the stem cell niche critically depends on Thr metabolism, and that when disturbed the normal continuum of cell states becomes aborted.