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    Deciphering the physiological and molecular functions of phytohormones
    (Elsevier B.V., 2023) Sharma, Manvi; Laxmi, Ashverya
    Plants rely on a diverse set of small molecules called phytohormones for growth, development, and adaptability. Since the discovery of auxin, hormones have been at the frontier of plant biology. Classically, hormone functions and responses were studied using synthetic hormones and analogs. However, the advent of technology, multidisciplinary approaches, and the genome sequencing of the model system of Arabidopsis and rice has dramatically increased our understanding of physiological and molecular mechanisms driving plant hormone actions. In this chapter, we talk about how independent or combined molecular action of phytohormones such as with their signaling components and regulators leads to changes in plant physiology to regulate multiple aspects of plant development, defense, and adaptation. We envisage that such detailed knowledge will allow a far greater understanding of the complex dynamics underlying plant hormone action.
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    A glucose-target of rapamycin signaling axis integrates environmental history of heat stress through maintenance of transcription-associated epigenetic memory in Arabidopsis
    (Oxford University Press, 2022) Sharma, Mohan; Sharma, Manvi; Jamsheer, Muhammed K; Laxmi, Ashverya
    In nature, plants cope with adversity and have established strategies that recall past episodes and enable them to better cope with stress recurrences by establishing a 'stress memory'. Emerging evidence suggests that Glucose (Glc) and Target of Rapamycin (TOR), central regulators of plant growth have remarkable functions in stress adaptation. However, whether TOR modulates a stress memory response is so far unknown. Global transcriptome profiling identified that Glc through TOR regulates the expression of numerous genes involved in thermomemory. Priming of TOR overexpressors with mild heat showed better stress endurance, whereas TOR RNAi showed reduced thermomemory. This thermomemory is linked with histone methylation at specific sites of heat stress (HS) genes. TOR promotes long-term accumulation of H3K4me3 on thermomemory-associated gene promoters, even when transcription of those genes reverts to their basal level. Our results suggest that ARABIDOPSIS TRITHORAX 1 (ATX1), an H3K4 methyltransferase already shown to regulate H3K4me3 levels at the promoters of HS recovery genes, is a direct target of TOR signaling. The TOR activating E2Fa binds to the promoter of ATX1, regulates its expression which ultimately regulates thermomemory. Collectively, our findings reveal a mechanistic framework in which Glc-TOR signaling determines the integration of stress and energy signaling to regulate thermomemory.
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    A negative feedback loop of TOR signaling balances growth and stress-response trade-offs in plants
    (Cell Press, 2022) Jamsheer, Muhammed K; Jindal, Sunita; Sharma, Mohan; Awasthi, Prakhar; S, Sreejath; Sharma, Manvi; Mannully, Chanchal Thomas; Laxmi, Ashverya
    TOR kinase is a central coordinator of nutrient-dependent growth in eukaryotes. Maintaining optimal TOR signaling is critical for the normal development of organisms. In this study, we describe a negative feedback loop of TOR signaling helping in the adaptability of plants in changing environmental conditions. Using an interdisciplinary approach, we show that the plant-specific zinc finger protein FLZ8 acts as a regulator of TOR signaling in Arabidopsis. In sugar sufficiency, TOR-dependent and -independent histone modifications upregulate the expression of FLZ8. FLZ8 negatively regulates TOR signaling by promoting antagonistic SnRK1α1 signaling and bridging the interaction of SnRK1α1 with RAPTOR1B, a crucial accessory protein of TOR. This negative feedback loop moderates the TOR-growth signaling axis in the favorable condition and helps in the activation of stress signaling in unfavorable conditions, establishing its importance in the adaptability of plants.
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    Jasmonic acid coordinates with light, glucose and auxin signalling in regulating branching angle of Arabidopsis lateral roots
    (John Wiley & Sons, 2022) Sharma, Manvi; Sharma, Mohan; Jamsheer, K. Muhammed; Laxmi, Ashverya
    The role of jasmonates (JAs) in primary root growth and development and in plant response to external stimuli is already known. However, its role in lateral root (LR) development remains to be explored. Our work identified methyl jasmonate (MeJA) as a key phytohormone in determining the branching angle of Arabidopsis LRs. MeJA inclines the LRs to a more vertical orientation, which was dependent on the canonical JAR1-COI1-MYC2,3,4 signalling. Our work also highlights the dual roles of light in governing LR angle. Light signalling enhances JA biosynthesis, leading to erect root architecture; whereas, glucose (Glc) induces wider branching angles. Combining physiological and molecular assays, we revealed that Glc antagonizes the MeJA response via TARGET OF RAPAMYCIN (TOR) signalling. Moreover, physiological assays using auxin mutants, MYC2-mediated transcriptional activation of LAZY2, LAZY4 and auxin biosynthetic gene CYP79B2,and asymmetric distribution of DR5::GFP and PIN2::GFP pinpointed the role of an intact auxin mechanism required by MeJA for vertical growth of LRs. We also demonstrated that light perception and signalling are indispensable for inducing vertical angles by MeJA. Thus, our investigation highlights antagonism between light and Glc signalling and how they interact with JA-auxin signals to optimize the branching angle of LRs.
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    Balancing growth and defense: Role of target of rapamycin and SNF1-related protein kinase 1 in stress signaling in plants
    (John Wiley & Sons, 2021) Sharma, Mohan; Jamsheer, K. Muhammed; Saksena, Harshita B.; Jindal, Sunita; Sharma, Manvi; Singh, Dhriti; Tiwari, Archna; Awasthi, Prakhar; Laxmi, Ashverya
    Plants have to maintain the growth and at the same time need to be vigilant about the imminent threat such as pathogen attack and unfavorable growth conditions. It is been observed that the energy status of the plant is an important determinant of the response to stress factors. The Target Of Rapamycin (TOR) and SNF1-Related Protein Kinase 1 (SnRK1) are serine/threonine kinases that originated early in the eukaryotic evolution, work as energy gauges in all eukaryotic lineages. During favorable growth conditions, the nutrient abundance activates TOR, which promotes growth through activation of general protein translation and cell cycle progression. The stress conditions can severely limit energy production, which can activate SnRK1 signaling. By inhibiting TOR kinase and through other effector proteins, the SnRK1 pathway enables the plants to survive in unfavorable growth conditions. The past decade opened a floodgate of studies regarding TOR and SnRK1 interaction regulating growth-defense trade-offs and stress mitigation. This also opened avenues for the utilization of these pathways for crop improvement. This chapter will succinctly summarize the current knowledge in this field and discuss the future direction of research.
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    Arabidopsis target of rapamycin coordinates with transcriptional and epigenetic machinery to regulate thermotolerance
    (Frontiers Media S.A., 2021) Sharma, Mohan; Jamsheer, K.M.; Shukla, Brihaspati Narayan; Sharma, Manvi; Awasthi, Prakhar; Mahtha, Sanjeet Kumar; Yadav, Gitanjali; Laxmi, Ashverya
    Global warming exhibits profound effects on plant fitness and productivity. To withstand stress, plants sacrifice their growth and activate protective stress responses for ensuring survival. However, the switch between growth and stress is largely elusive. In the past decade, the role of the target of rapamycin (TOR) linking energy and stress signalling is emerging. Here, we have identified an important role of Glucose (Glc)-TOR signalling in plant adaptation to heat stress (HS). Glc via TOR governs the transcriptome reprogramming of a large number of genes involved in heat stress protection. Downstream to Glc-TOR, the E2Fa signalling module regulates the transcription of heat shock factors through direct recruitment of E2Fa onto their promoter regions. Also, Glc epigenetically regulates the transcription of core HS signalling genes in a TOR-dependent manner. TOR acts in concert with p300/CREB HISTONE ACETYLTRANSFERASE1 (HAC1) and dictates the epigenetic landscape of HS loci to regulate thermotolerance. Arabidopsis plants defective in TOR and HAC1 exhibited reduced thermotolerance with a decrease in the expression of core HS signalling genes. Together, our findings reveal a mechanistic framework in which Glc-TOR signalling through different modules integrates stress and energy signalling to regulate thermotolerance.
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    Understanding the intricate web of phytohormone signalling in modulating root system architecture
    (MDPI AG, 2021) Sharma, Manvi; Singh, Dhriti; Saksena, Harshita B.; Sharma, Mohan; Tiwari, Archna; Awasthi, Prakhar; Botta, Halidev Krishna; Shukla, Brihaspati Narayan; Laxmi, Ashverya
    Root system architecture (RSA) is an important developmental and agronomic trait that is regulated by various physical factors such as nutrients, water, microbes, gravity, and soil compaction as well as hormone-mediated pathways. Phytohormones act as internal mediators between soil and RSA to influence various events of root development, starting from organogenesis to the formation of higher order lateral roots (LRs) through diverse mechanisms. Apart from interaction with the external cues, root development also relies on the complex web of interaction among phytohormones to exhibit synergistic or antagonistic effects to improve crop performance. However, there are considerable gaps in understanding the interaction of these hormonal networks during various aspects of root development. In this review, we elucidate the role of different hormones to modulate a common phenotypic output, such as RSA in Arabidopsis and crop plants, and discuss future perspectives to channel vast information on root development to modulate RSA components.
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    The versatile role of glucose signalling in regulating growth, development and stress responses in plants
    (Springer Nature Publishing AG, 2020) Saksena, Harshita B.; Sharma, Manvi; Singh, Dhriti; Laxmi, Ashverya
    Sugars as an energy source and a signalling molecule are indispensible for growth, development and stress responses in plants. Among sugars, glucose (Glc) has been identified to perform a key role in regulating various cellular and developmental processes in plants. This comprehensive review highlights the crosstalk of glucose signalling with auxin, cytokinin and brassinosteroid signalling in controlling several aspects of plant development including root growth deviation, root waving and coiling, lateral root emergence, hypocotyl elongation, etc. through a Hexokinase 1 dependent and independent pathway in Arabidopsis. It also provides an insight on the role of Glc-mediated target of rapamycin signalling in modulating various abiotic stresses like nutrient deficiency stress, heat stress, oxidative stress etc. The review also discusses about sugar inducible FCS-Like Zinc Finger genes in modulating SNF1-related protein kinase 1 signalling to coordinate growth and stress responses in plants. Therefore, glucose signalling in concert with diverse signalling pathways and via regulating certain genes contributes to numerous cellular processes to control development and stress responses in plants.
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    The FCS-LIKE ZINC FINGER 6 and 10 are involved in regulating osmotic stress responses in Arabidopsis
    (Taylor & Francis Group, 2019) Jamsheer, K Muhammed; Singh, Dhriti; Sharma, Mohan; Sharma, Manvi; Jindal, Sunita; Mannully, Chanchal T.; Shukla, Brihaspati N.; Laxmi, Ashverya
    The TARGET OF RAPAMYCIN-SNF1-RELATED PROTEIN KINASE 1 (TOR-SnRK1) arms race is a key regulator of plant growth in response to energy fluctuations and stress. Recently, we have identified that two members of the FCS-LIKE ZINC FINGER (FLZ) protein family, FLZ6 and 10, repress SnRK1 signaling and thereby involved in the activation of the TARGET OF RAPAMYCIN (TOR) signaling. In this study, we demonstrate that FLZ6 and 10 are also involved in the regulation of osmotic stress responses. Downregulation of FLZ6 and 10 results in enhanced expression of stress-responsive genes and better resilience towards osmotic stress at the seedling stage. These results indicate that FLZ6 and 10 are involved in the regulation of stress mitigation in plants through directly affecting SnRK1 signaling.
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    FCS-like zinc finger 6 and 10 repress SnRK1 signalling in Arabidopsis
    (John Wiley & Sons, 2018) Jamsheer, Muhammed K.; Sharma, Manvi; Singh, Dhriti; Mannully, Chanchal Thomas; Jindal, Sunita; Shukla, Brihaspati Narayan; Laxmi, Ashverya
    SNF1-Related Protein Kinase 1 (SnRK1) is a central regulator of plant growth during energy starvation. The FCS-Like Zinc finger (FLZ) proteins are recently identified adaptor proteins which facilitate the interaction of SnRK1 with other proteins. In this study, we identified that two starvation-induced FLZ genes, FLZ6 and FLZ10, work as repressors of SnRK1 signalling. The reduced expression of these genes resulted in an increase in the level of SnRK1α1, which is the major catalytic subunit of SnRK1. This resulted in a concomitant increase in the phosphorylated protein and SnRK1 activity in the flz6 and flz10 mutants. FLZ6 and FLZ10 specifically interact with SnRK1α subunits in the cytoplasmic foci which colocalized with the endoplasmic reticulum. In physiological assays, similar to SnRK1α1 overexpression line, flz mutants showed compromised growth. Further, the growth promotion in response to favourable growth conditions was found to be attenuated in the mutants. The enhanced SnRK1 activity in the mutants resulted in a reduction in the level of phosphorylated RIBOSOMAL S6 KINASE and the expression of E2Fa and its targets indicating that TARGET OF RAPAMYCIN-dependent promotion of protein synthesis and cell cycle progression is impaired. Taken together, this study uncovers a plant-specific modulation of SnRK1 signalling.