Institutional Publications
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Item Type-A response regulators negatively mediate heat stress response by altering redox homeostasis in Arabidopsis(Frontiers Media S.A., 2022) Jindal, Sunita; Kerchev, Pavel; Berka, Miroslav; Černý, Martin; Botta, Halidev Krishna; Laxmi, Ashverya; Brzobohatý, BřetislavBesides the long-standing role of cytokinins (CKs) as growth regulators, their current positioning at the interface of development and stress responses is coming into recognition. The current evidence suggests the notion that CKs are involved in heat stress response (HSR), however, the role of CK signaling components is still elusive. In this study, we have identified a role of the CK signaling components type-A Arabidopsis response regulators (ARRs) in HSR in Arabidopsis. The mutants of multiple type-A ARR genes exhibit improved basal and acquired thermotolerance and, altered response to oxidative stress in our physiological analyses. Through proteomics profiling, we show that the type-A arr mutants experience a 'stress-primed' state enabling them to respond more efficiently upon exposure to real stress stimuli. A substantial number of proteins that are involved in the heat-acclimatization process such as the proteins related to cellular redox status and heat shock, are already altered in the type-A arr mutants without a prior exposure to stress conditions. The metabolomics analyses further reveal that the mutants accumulate higher amounts of α-and γ-tocopherols, which are important antioxidants for protection against oxidative damage. Collectively, our results suggest that the type-A ARRs play an important role in heat stress response by affecting the redox homeostasis in Arabidopsis.Item 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, AshveryaTOR 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.Item 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, AshveryaPlants 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.Item 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, AshveryaThe 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.Item Evolution of TOR-SnRK dynamics in green plants and its integration with phytohormone signaling networks(Oxford University Press, 2019) Jamsheer, K Muhammed; Jindal, Sunita; Laxmi, AshveryaThe Target Of Rapamycin-SNF1-Related Protein Kinase 1 (TOR-SnRK1) arms race is an ancient regulatory mechanism evolved in eukaryotes to regulate nutrient-dependent growth. The autotrophic nature makes plants a distinct class in the eukaryotic lineage. Although TOR-SnRK1 signaling cascade shows highly conserved functions, studies in the past two decades identified many important plant-specific innovations in this pathway. Plants also possess SnRK2 and SnRK3 kinases which are originated from the ancient SnRK1-related kinases and do specialized functions in controlling growth, stress responses and nutrient homeostasis in plants. Recently, an integrative picture has started to emerge where different SnRKs and TOR kinase are highly interconnected to control nutrient and stress responses of plants. Further, these kinases are intimately involved with phytohormone signaling networks which originated at different stages of plant evolution. In this review, we are highlighting the evolution and divergence of TOR-SnRKs signaling components in plants and their communication between each other and phytohormone signaling to fine-tune growth and stress responses in plants.Item The FCS-like zinc finger scaffold of the kinase SnRK1 is formed by the coordinated actions of the FLZ domain and intrinsically disordered regions(The American Society for Biochemistry and Molecular Biology, 2018) Jamsheer, K Muhammed; Shukla, Brihaspati N.; Jindal, Sunita; Gopan, Nandu; Mannully, Chanchal Thomas; Laxmi, AshveryaThe SNF1-related protein kinase 1 (SnRK1) is a heterotrimeric eukaryotic kinase that interacts with diverse proteins and regulates their activity in response to starvation and stress signals. Recently, the FCS-like zinc finger (FLZ) proteins were identified as a potential scaffold for SnRK1 in plants. However, the evolutionary and mechanistic aspect of this complex formation is currently unknown. Here, in silico analyses predicted that FLZ proteins possess conserved intrinsically disordered regions (IDRs) with a propensity for protein binding in the N and C termini across the plant lineage. We observed that the Arabidopsis FLZ proteins promiscuously interact with SnRK1 subunits, which formed different isoenzyme complexes. The FLZ domain was essential for mediating the interaction with SnRK1α subunits, whereas the IDRs in the N termini facilitated interactions with the β and βγ subunits of SnRK1. Furthermore, the IDRs in the N termini were important for mediating dimerization of different FLZ proteins. Of note, the interaction of FLZ with SnRK1 was confined to cytoplasmic foci, which colocalized with the endoplasmic reticulum. An evolutionary analysis revealed that in general, the IDR-rich regions are under more relaxed selection than the FLZ domain. In summary, the findings in our study reveal the structural details, origin, and evolution of a land plant–specific scaffold of SnRK1 formed by the coordinated actions of IDRs and structured regions in the FLZ proteins. We propose that the FLZ protein complex might be involved in providing flexibility, thus enhancing the binding repertoire of the SnRK1 hub in land plants.Item 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, AshveryaSNF1-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.