Unveiling the significance of Target of Rapamycin (TOR) sign

PERSPECTIVE   Open Access    

Unveiling the significance of Target of Rapamycin (TOR) signalling in grafting

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1.

Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, China Agricultural University, Beijing 100193, China

2.

Institute de Biologie Moléculaire des Plantes, Centre National de la Recherche Scientifique, UPR 2357, Université de Strasbourg, Strasbourg 67084, France

3.

Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao 266101, China

4.

Shandong Energy Institute, Qingdao 266101, China

5.

Qingdao New Energy Shandong Laboratory, Qingdao 266101, China

6.

Shanghai Waker Bioscience Co., Ltd, Shanghai 201114, China

Received: 11 September 2023

Revised: 11 December 2023

Accepted: 03 January 2024

Published online: 31 January 2024

Vegetable Research  4,  Article number: e004  (2024)  | 

Abstract: Grafting is a widely employed horticultural technique that enables the combination of desirable traits from different plant species or cultivars. The success of grafting depends on various factors, including the strength of the seedlings, proper healing of the grafting junction, and the subsequent recovery of heterografted seedlings. In recent years, the target of rapamycin (TOR), a conserved protein kinase, has emerged as a key regulator of growth and development in plants. This perspective paper delves into the implications of TOR signalling in the grafting processes, including the role of the TOR signalling pathway in the regulation of seedling vigour prior to grafting, healing of graft junction and shoot-to-root communications. Particularly, we highlight the role of gibberellin and m5C modification in the regulatory network of TOR. However, further research is needed to unravel the precise molecular mechanisms underlying TOR's involvement in grafting and to optimize its application for improved grafting outcomes.

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HTML Introduction

Grafting, a time-honoured horticultural technique, has revolutionized plant breeding and cultivation by enabling the combination of desirable traits from different plant species or cultivars[]. The success of grafting relies on various factors, including the strength of the seedlings, proper healing of the grafting junction, and the subsequent recovery of heterografted seedlings[]. Recent advancements in our understanding of the target of rapamycin (TOR) signalling pathway have shed light on its pivotal role in regulating growth and development in plants[]. As an evolutionarily conserved protein kinase, TOR integrates diverse signals and coordinates cellular processes related to growth, nutrient signalling, and stress responses. In this perspective paper, we delve into the implications of TOR signalling in grafting, exploring its involvement in pre-grafting growth regulation, graft healing at the junction site, and the possible mechanisms underlying the shoot-root communication in heterografted seedlings. By elucidating the contributions of TOR signalling to grafting processes, we aim to provide valuable insights that can enhance grafting success rates and broaden the scope of agricultural practices and crop improvement strategies.

Pre-grafting growth regulation by TOR TOR's potential role in healing the grafting junction

Grafting is a process that involves the fusion and subsequent healing of two plant tissues. Successful wound healing during grafting relies on the formation of callus cells. TOR plays a crucial role in regulating the activation of various genes and pathways involved in cell proliferation, differentiation, and tissue regeneration. Additionally, TOR signalling has been strongly implicated in wound healing and callus formation in plants[−]. Notably, two TOR-downstream pathways have demonstrated significant capability in regulating callus formation and cell differentiation. TOR promotes anabolic processes, such as translation, while inhibiting catabolic processes, like autophagy[]. Studies involving autophagy mutants have shown that impaired autophagy severely hampers cell differentiation[]. Moreover, the TOR-Polycomb repressive complex 2 (PRC2) pathway has recently emerged as a core regulator of plant development and stress responses[,]. Severe PRC2 mutants, such as fie and clf/swn double mutants, exhibit a callus-like phenotype, indicating the significance of this pathway in regulating cell differentiation during wound healing[]. However, the specific involvement of TOR in this process remains unclear.

Both sugar and auxin, the most characterized TOR activators, have been studied most in details regarding their systemic roles in tissue regeneration after wounding[,]. In the context of grafting, TOR signalling promotes sugar-mediated callus formation at the grafting junction, which is a vital step in successful graft healing[,,]. In the study by Xiong et al., the role of TOR in graft junction healing was initially characterized using rapamycin-sensitive BP12 lines, contrasting with the rapamycin insensitivity observed in wild-type Arabidopsis. Notably, self-grafting of BP12-2 proved unattainable in the presence of rapamycin, underscoring the pivotal role of TOR in graft junction formation[]. This observation was subsequently corroborated by Miao et al. in the widely utilized cucumber-pumpkin grafting system. An intriguing aspect of their approach involved employing sugar-starved etiolated seedlings for grafting. The introduction of exogenous glucose significantly heightened the grafting success rate. It is noteworthy, however, that xylem reconnection induced by sugar appears to be TOR-independent in cucumber-pumpkin heterografts[].

During graft formation, auxin is necessary for re-establishing severed vasculature by promoting callus growth and forming new vascular connections between scion and rootstock[]. While shoot-derived auxin was initially thought to be the primary driver of graft formation[], recent evidence suggests a more complex scenario. Systemic auxin flow appears not to corelate with vascular regeneration[], but environmental conditions can influence the process through remote signals, affecting proliferation at the graft site[]. A systemic increase in auxin levels induced by elevated temperature had a promotive effect on proliferation at the graft site, leading to faster connections of grafted tomatoes[]. Additionally, cotyledon-derived auxin does not seem to play a major role in vasculature regeneration[]. However, the role of TOR in auxin-mediated graft healing remains elusive.

Scion-rootstock communicaTOR after grafting Limitations and outlooks

TOR serves as a pivotal master regulator orchestrating plant growth and developmental processes by assimilating a multitude of upstream signals and finely modulating crucial downstream cellular mechanisms, encompassing translation, autophagy, and the cell cycle[]. While the scrutiny of this kinase has been exhaustive within metazoans, its comprehensive exploration within the plant kingdom commenced notably later, specifically around 2017. To this day, a distinct comprehension of TOR's multifaceted functionality remains constrained, primarily attributable to the dearth of diverse mutants and reporter lines, particularly in non-Arabidopsis plant species. This perspective paper seeks to illuminate the latent role of TOR in the grafting process, with the overarching goal of directing heightened research focus towards the TOR signalling pathway within the realm of vegetable crops.

Although the characterization of TOR as a conserved kinase across eukaryotes is well-established, its functional implications might diverge considerably. Notably, TOR signalling pathways undergo a complete reprogramming in photoautotrophic organisms compared to their heterotrophic counterparts[,]. Intriguingly, recent research has unveiled pivotal insertions within the TOR protein of salamanders, correlating with their remarkable regenerative capabilities in contrast to mammals[]. This raises the intriguing possibility of an augmented regenerative role for plant TOR during the course of evolution, considering a low amino acid sequence identity of Arabidopsis TOR, especially at the N-terminus, compared to its animal counterparts[]. This tantalizing perspective holds significant promise, particularly within vegetable crops subject to multiple annual harvests and in the context of grafting junction healing. Another study in vegetable crops highlights an intriguing future perspective on TOR signalling. The absence of a plant TOR inhibitor posed a significant challenge for TOR research in past decades, given the insensitivity of most studied higher plants to rapamycin due to the non-functional FK506 Binding Protein 12 KD (FKBP12). Intriguingly, in horticultural crops such as tomatoes, SlFKBP12 can facilitate the inhibitory interaction between rapamycin and TOR, mirroring the situation observed in yeast and mammals[]. The delineation of a comprehensive phylogenetic analysis coupled with an in-depth functional evolution study on TOR and its signalling components emerges as an imperative avenue for future research endeavours.

TOR plays a crucial role in orchestrating efficient shoot-to-root communication by coordinating nutrient and phytohormone signalling. However, research on TOR in vegetable crops, particularly in the context of heterografts, is noticeably limited. This is particularly intriguing given that specific rootstocks have the potential to enhance various agricultural traits in scions including increased stress tolerance and fruit yield[]. Exploring how the TOR signalling pathway in the scion might be reprogrammed by a specific rootstock becomes an intriguing avenue of inquiry. Furthermore, TOR itself could potentially serve as a conduit for shoot-to-root communication. Notably, within animal systems, the mobility of TOR mRNA has been observed during nerve injury[]. While such mobility hasn't been observed in Arabidopsis[], recent advancements in mobile RNA databases, specifically in the context of cucumber (Csa)/pumpkin (Cmo) heterografts, have unveiled CsaTOR (CsGy7G006260) and CmoTOR (CmoCh19G005520) as mobile shoot-to-root transcripts. Remarkably, CmoTOR has been identified as being modified by m5C in the vascular extrude[]. This intriguing discovery raises the tantalizing prospect that TOR mRNA mobility might indeed be a phenomenon that varies across diverse plant species.

To gain comprehensive insights into this dynamic, it becomes imperative to delve into the regulation of TOR mRNA transcription, a facet that presently remains strikingly unexplored. During tomato fruit ripening, TOR is silenced transcriptionally to promote ethylene production[,]. However, the mechanism remains obscure. The only known instance of a well-studied transcription factor from the jasmonic acid (JA) signalling pathway, MYC2, binding to the promoter region of TOR has been identified in tomatoes[]. Unravelling the intricacies of this transcriptional control is pivotal in comprehending the potential mobility of TOR mRNA within heterografts. By bridging this gap in knowledge, we can not only expand our understanding of TOR's communication capabilities but also pave the way for unlocking the underlying mechanisms governing shoot-to-root signalling in the intricate context of plant grafting.

Author contributions

The authors confirm contribution to the paper as follows: Zhang W, Han L, Dong Y initiated the project and designed the experiments; Zhang W, Huang Y, He J, Dong Y performed experiments; Huang Y, He J were supervised by Zhang W. Zhang W, Dong Y made figures and wrote the manuscript; Han L, He F revised the manuscript. All authors reviewed the results and approved the final version of the manuscript.

Data availability

All data generated or analyzed during this study are included in this published article.

Acknowledgments

We thank Dr. C. Meyer (INRAE, France) for providing the 35-7 line, Dr. Y. Zhou for providing the dnmt2 nsun2b mutant, the ikann-editorial team for language editing (ikann-editing@outlook.com), the 2020 Marie-Curie fellowship 885864 TOR in acTIon MSCA-IF-EF-ST to Y. Dong, and the 2115 Talent Development Program of China Agricultural University to W. Zhang.

Conflict of interest

The authors declare that they have no conflict of interest.

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Cite this article

Zhang W, Han L, Huang Y, He J, He F, et al. 2024. Unveiling the significance of Target of Rapamycin (TOR) signalling in grafting. Vegetable Research 4: e004 doi: 10.48130/vegres-0024-0003

Zhang W, Han L, Huang Y, He J, He F, et al. 2024. Unveiling the significance of Target of Rapamycin (TOR) signalling in grafting. Vegetable Research 4: e004 doi: 10.48130/vegres-0024-0003