Umeå Plant Science Centre - Pandey, Shashank - Decoding the molecular control of bud dormancy release in trees

Research

Shashank Pandey is standing in a greenhouse with small aspen trees on a table in front of him and taller ones behind him, he is looking straight in the camera

Photo: Jasim Basheer

The DECORE project aims to uncover mechanisms by which low temperature controls bud dormancy in hybrid aspen. Recent research in our lab identified AGL8 as a transcription factor involved in the release of bud dormancy. Building on this, we hypothesize that AGL8 regulates gibberellin, the mobile signaling component FT1, and intercellular communication to coordinate the release of bud dormancy.

Plants have an astonishing ability to sense and respond to environmental cues, including seasonal changes. One critical but poorly understood aspect of this responsiveness is the regulation of bud dormancy in trees, a phenomenon central to their survival and growth in temperate regions. My MSCA research, focusing on the experimental model tree hybrid aspen, endeavours to shed light on the intricate mechanisms behind the control of plant development by seasonal cues, especially those related to temperature-mediated bud dormancy.

In temperate and boreal regions, perennial plants experience temperature extremes, from freezing winters to warm summers. To survive, they employ sophisticated mechanisms that detect seasonal variations and adjust their growth accordingly (Fig 1). In late summer, short days trigger the cessation of growth and protect the shoot apical meristem (SAM) and leaf primordia in a bud from winter damage. Dormancy is established to prevent early growth activation until favourable conditions return in spring. As spring arrives, dormancy is released, enabling bud break and initiating the growth cycle (Fig 1). However, the molecular mechanism underlying bud dormancy release has remained a mystery. Recent research has uncovered a novel mechanism involving the control of cell-cell communication via plasmodesmata (PDs), which are intercellular channels responsible for the trafficking of growth regulators. This dynamic regulation of PDs plays a vital role in bud dormancy.

Schematic overview about the dormancy cycle in the apex of aspen: five photos arranged in a circle with arrows inbetween llustrate how the apex looks like at the different stages during the season. Additional information describing the stage of the respective stage is added to each arrow.

Fig. 1: Seasonal changes occurring in the apex of hybrid aspen during dormancy
Under long-day (LD) and warm temperature (WT) conditions in the summer, trees grow actively and stop their growth upon sensing short-days (SDs) during early autumn. SDs induce dormancy in the buds in late autumn. Chilling temperatures (LT) during the winter periods promote the release of dormancy. Relatively warmer temperature in the spring promotes the bud burst, followed by active growth again in the summer.

The identification of key genes and factors, including AGL8, FT1, GA-20 oxidase, and the callose-degrading enzyme GH17, as downstream targets of AGL8, provides a unique opportunity to unravel the relationship between gene regulation, hormonal changes, cell-cell communication (via PDs), and their combined role in temperature-mediated bud dormancy control. Based on this, the research project has below objectives:

Elucidating the role of AGL8-mediated FT1 activation in inducing the release of bud dormancy

This objective aims to investigate if FT1 is a downstream target of AGL8 and if so, uncover the significance of FT1 regulation by AGL8 in the release of bud dormancy (Fig. 2). This objective involves utilization of Chromatin Immuno-Precipitation PCR (ChIP-PCR) technique to probe the interaction between AGL8 and the FT1 promoter, which is essential for confirming AGL8 binding to the FT1 promoter. Next, AGL8-overexpressing plants carrying FT1 loss-of-function mutations (AGL8ox/ft1) will be created using CRISPR-Cas9 technology. Finally, dormancy release in the AGL8ox/ft1 double mutant and the AGL8-overexpressing parental line (AGL8ox) is compared using controlled growth conditions, simulating transitions to autumn and winter followed by bud break observation.

Determination of AGL8’s role in hormonal control of bud dormancy release in response to temperature cues

This objective delves into the role of AGL8 in regulating gibberellic acid (GA) biosynthesis, a key hormonal factor influencing bud dormancy release (Fig. 2). It involves measurement of GA levels in buds from wild-type (wt), AGL8-overexpressing (AGL8ox), and AGL8-RNAi plants after dormancy release to assess AGL8's impact on GA biosynthesis. Following that, we will introduce cDNA for GA-2 oxidase, a GA-degrading enzyme, into WT and AGL8ox hybrid aspen plants. Then we will analyse dormancy release in WT and AGL8ox lines expressing GA-2 oxidase under controlled growth conditions to determine the role of GA in low-temperature-induced dormancy release. The expected outcomes of these investigations include insights into AGL8's role as a regulator of GA biosynthesis and its significance in controlling dormancy release in response to low temperatures.

Uncovering the role of AGL8-regulated PD opening in bud dormancy release

It focuses on the role of PDs and their connection to bud dormancy (Fig. 2). We aim to understand if AGL8, a key gene identified in our research, activates GH17, an enzyme linked to the breakdown of callose, which in turn opens the PDs, enabling dormancy release by employing employ transmission electron microscopy and immunogold labelling approaches.

Scheme illustrating the key objectives of the research project: Identifying how low temperature regulates dormancy release through AGL8 FT1 activation (objective !), GA biosynthesis (objective 2) and opening of plasmodesmata (objective 3)

Fig. 2: Key project objectives to elucidate the dormancy release.

In summary, this research project seeks to unravel the mysteries behind bud dormancy in trees by investigating the interactions between genes, hormones, and cell-cell communication. The findings will not only advance our understanding of how plants adapt to seasonal changes but will also contribute to the competitiveness of European research, particularly in the field of developmental adaptation to seasonal variations.

This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 101025929.

CV S. K. Pandey

Publications

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2024 (2)

A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release. Pandey, S. K, Maurya, J. P., Aryal, B., Drynda, K., Nair, A., Miskolczi, P., Singh, R. K., Wang, X., Ma, Y., de Souza Moraes, T., Bayer, E. M, Farcot, E., Bassel, G. W, Band, L. R, & Bhalerao, R. P The EMBO Journal, 43(23): 5793–5812. December 2024. Num Pages: 5812 Publisher: John Wiley & Sons, Ltd

A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release [link]

Paper doi link bibtex abstract

@article{pandey_regulatory_2024,
	title = {A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release},
	volume = {43},
	issn = {0261-4189},
	url = {https://www.embopress.org/doi/full/10.1038/s44318-024-00256-5},
	doi = {10.1038/s44318-024-00256-5},
	abstract = {The control of cell–cell communication via plasmodesmata (PD) plays a key role in plant development. In tree buds, low-temperature conditions (LT) induce a switch in plasmodesmata from a closed to an open state, which restores cell-to-cell communication in the shoot apex and releases dormancy. Using genetic and cell-biological approaches, we have identified a previously uncharacterized transcription factor, Low-temperature-Induced MADS-box 1 (LIM1), as an LT-induced, direct upstream activator of the gibberellic acid (GA) pathway. The LIM1-GA module mediates low temperature-induced plasmodesmata opening, by negatively regulating callose accumulation to promote dormancy release. LIM1 also activates expression of FT1 (FLOWERING LOCUS T), another LT-induced factor, with LIM1-FT1 forming a coherent feedforward loop converging on low-temperature regulation of gibberellin signaling in dormancy release. Mathematical modeling and experimental validation suggest that negative feedback regulation of LIM1 by gibberellin could play a crucial role in maintaining the robust temporal regulation of bud responses to low temperature. These results reveal genetic factors linking temperature control of cell–cell communication with regulation of seasonally-aligned growth crucial for adaptation of trees.},
	number = {23},
	urldate = {2024-12-06},
	journal = {The EMBO Journal},
	author = {Pandey, Shashank K and Maurya, Jay Prakash and Aryal, Bibek and Drynda, Kamil and Nair, Aswin and Miskolczi, Pal and Singh, Rajesh Kumar and Wang, Xiaobin and Ma, Yujiao and de Souza Moraes, Tatiana and Bayer, Emmanuelle M and Farcot, Etienne and Bassel, George W and Band, Leah R and Bhalerao, Rishikesh P},
	month = dec,
	year = {2024},
	note = {Num Pages: 5812
Publisher: John Wiley \& Sons, Ltd},
	keywords = {Callose, Dormancy, Gibberellins, Plasmodesmata, Temperature},
	pages = {5793--5812},
}

Molecular advances in bud dormancy in trees. Ding, J., Wang, K., Pandey, S., Perales, M., Allona, I., Khan, M. R. I., Busov, V. B, & Bhalerao, R. P Journal of Experimental Botany, 75(19): 6063–6075. October 2024.

Molecular advances in bud dormancy in trees [link]

Paper doi link bibtex abstract

@article{ding_molecular_2024,
	title = {Molecular advances in bud dormancy in trees},
	volume = {75},
	issn = {0022-0957},
	url = {https://doi.org/10.1093/jxb/erae183},
	doi = {10.1093/jxb/erae183},
	abstract = {Seasonal bud dormancy in perennial woody plants is a crucial and intricate process that is vital for the survival and development of plants. Over the past few decades, significant advancements have been made in understanding many features of bud dormancy, particularly in model species, where certain molecular mechanisms underlying this process have been elucidated. We provide an overview of recent molecular progress in understanding bud dormancy in trees, with a specific emphasis on the integration of common signaling and molecular mechanisms identified across different tree species. Additionally, we address some challenges that have emerged from our current understanding of bud dormancy and offer insights for future studies.},
	number = {19},
	urldate = {2024-10-18},
	journal = {Journal of Experimental Botany},
	author = {Ding, Jihua and Wang, Kejing and Pandey, Shashank and Perales, Mariano and Allona, Isabel and Khan, Md Rezaul Islam and Busov, Victor B and Bhalerao, Rishikesh P},
	month = oct,
	year = {2024},
	pages = {6063--6075},
}

2023 (1)

LBD18 and IAA14 antagonistically interact with ARF7 via the invariant Lys and acidic residues of the OPCA motif in the PB1 domain. Nguyen, U. T., Pandey, S. K., & Kim, J. Planta, 258(2): 26. June 2023.

LBD18 and IAA14 antagonistically interact with ARF7 via the invariant Lys and acidic residues of the OPCA motif in the PB1 domain [link]

Paper doi link bibtex abstract

@article{nguyen_lbd18_2023,
	title = {{LBD18} and {IAA14} antagonistically interact with {ARF7} via the invariant {Lys} and acidic residues of the {OPCA} motif in the {PB1} domain},
	volume = {258},
	issn = {1432-2048},
	url = {https://doi.org/10.1007/s00425-023-04183-3},
	doi = {10.1007/s00425-023-04183-3},
	abstract = {LBD18 and IAA14 antagonistically interact with ARF7 through the electrostatic faces in the ARF7PB1 domain, modulating ARF7 transcriptional activity.},
	language = {en},
	number = {2},
	urldate = {2023-11-14},
	journal = {Planta},
	author = {Nguyen, Uyen Thu and Pandey, Shashank K. and Kim, Jungmook},
	month = jun,
	year = {2023},
	keywords = {ARF19, ARF7, Aux/IAA, Auxin response factor, LBD, Lateral organ boundaries domain, PB1 domain},
	pages = {26},
}

2022 (1)

Understanding the Modus Operandi of Class II KNOX Transcription Factors in Secondary Cell Wall Biosynthesis. Nookaraju, A., Pandey, S. K., Ahlawat, Y. K., & Joshi, C. P. Plants, 11(4): 493. January 2022. Number: 4 Publisher: Multidisciplinary Digital Publishing Institute

Understanding the Modus Operandi of Class II KNOX Transcription Factors in Secondary Cell Wall Biosynthesis [link]

Paper doi link bibtex abstract

@article{nookaraju_understanding_2022,
	title = {Understanding the {Modus} {Operandi} of {Class} {II} {KNOX} {Transcription} {Factors} in {Secondary} {Cell} {Wall} {Biosynthesis}},
	volume = {11},
	copyright = {http://creativecommons.org/licenses/by/3.0/},
	issn = {2223-7747},
	url = {https://www.mdpi.com/2223-7747/11/4/493},
	doi = {10.3390/plants11040493},
	abstract = {Lignocellulosic biomass from the secondary cell walls of plants has a veritable potential to provide some of the most appropriate raw materials for producing second-generation biofuels. Therefore, we must first understand how plants synthesize these complex secondary cell walls that consist of cellulose, hemicellulose, and lignin in order to deconstruct them later on into simple sugars to produce bioethanol via fermentation. Knotted-like homeobox (KNOX) genes encode homeodomain-containing transcription factors (TFs) that modulate various important developmental processes in plants. While Class I KNOX TF genes are mainly expressed in the shoot apical meristems of both monocot and eudicot plants and are involved in meristem maintenance and/or formation, Class II KNOXTF genes exhibit diverse expression patterns and their precise functions have mostly remained unknown, until recently. The expression patterns of Class II KNOX TF genes in Arabidopsis, namely KNAT3, KNAT4, KNAT5, and KNAT7, suggest that TFs encoded by at least some of these genes, such as KNAT7 and KNAT3, may play a significant role in secondary cell wall formation. Specifically, the expression of the KNAT7 gene is regulated by upstream TFs, such as SND1 and MYB46, while KNAT7 interacts with other cell wall proteins, such as KNAT3, MYB75, OFPs, and BLHs, to regulate secondary cell wall formation. Moreover, KNAT7 directly regulates the expression of some xylan synthesis genes. In this review, we summarize the current mechanistic understanding of the roles of Class II KNOX TFs in secondary cell wall formation. Recent success with the genetic manipulation of Class II KNOX TFs suggests that this may be one of the biotechnological strategies to improve plant feedstocks for bioethanol production.},
	language = {en},
	number = {4},
	urldate = {2023-11-14},
	journal = {Plants},
	author = {Nookaraju, Akula and Pandey, Shashank K. and Ahlawat, Yogesh K. and Joshi, Chandrashekhar P.},
	month = jan,
	year = {2022},
	note = {Number: 4
Publisher: Multidisciplinary Digital Publishing Institute},
	keywords = {KNOX II transcription factors, bioethanol, saccharification, secondary cell walls, xylan, xylem and fiber development},
	pages = {493},
}

2021 (1)

Recent advances in peptide signaling during Arabidopsis root development. Jeon, B. W., Kim, M., Pandey, S. K, Oh, E., Seo, P. J., & Kim, J. Journal of Experimental Botany, 72(8): 2889–2902. April 2021.

Recent advances in peptide signaling during Arabidopsis root development [link]

Paper doi link bibtex abstract

@article{jeon_recent_2021,
	title = {Recent advances in peptide signaling during {Arabidopsis} root development},
	volume = {72},
	issn = {0022-0957},
	url = {https://doi.org/10.1093/jxb/erab050},
	doi = {10.1093/jxb/erab050},
	abstract = {Roots provide the plant with water and nutrients and anchor it in a substrate. Root development is controlled by plant hormones and various sets of transcription factors. Recently, various small peptides and their cognate receptors have been identified as controlling root development. Small peptides bind to membrane-localized receptor-like kinases, inducing their dimerization with co-receptor proteins for signaling activation and giving rise to cellular signaling outputs. Small peptides function as local and long-distance signaling molecules involved in cell-to-cell communication networks, coordinating root development. In this review, we survey recent advances in the peptide ligand-mediated signaling pathways involved in the control of root development in Arabidopsis. We describe the interconnection between peptide signaling and conventional phytohormone signaling. Additionally, we discuss the diversity of identified peptide–receptor interactions during plant root development.},
	number = {8},
	urldate = {2023-11-14},
	journal = {Journal of Experimental Botany},
	author = {Jeon, Byeong Wook and Kim, Min-Jung and Pandey, Shashank K and Oh, Eunkyoo and Seo, Pil Joon and Kim, Jungmook},
	month = apr,
	year = {2021},
	pages = {2889--2902},
}

2019 (2)

LBD13 positively regulates lateral root formation in Arabidopsis. Cho, C., Jeon, E., Pandey, S. K., Ha, S. H., & Kim, J. Planta, 249(4): 1251–1258. April 2019.

LBD13 positively regulates lateral root formation in Arabidopsis [link]

Paper doi link bibtex abstract

@article{cho_lbd13_2019,
	title = {{LBD13} positively regulates lateral root formation in {Arabidopsis}},
	volume = {249},
	issn = {1432-2048},
	url = {https://doi.org/10.1007/s00425-018-03087-x},
	doi = {10.1007/s00425-018-03087-x},
	abstract = {Lateral Organ Boundaries Domain 13 (LBD13), which is expressed in emerged lateral roots and encodes a transcriptional activator, plays an important role in lateral root formation in Arabidopsis.},
	language = {en},
	number = {4},
	urldate = {2023-11-14},
	journal = {Planta},
	author = {Cho, Chuloh and Jeon, Eunkyeong and Pandey, Shashank K. and Ha, Se Hoon and Kim, Jungmook},
	month = apr,
	year = {2019},
	keywords = {Arabidopsis thaliana, LBD14, Lateral organ boundaries domain, Lateral root, Protoplasts, RNAi, Transcription factor},
	pages = {1251--1258},
}

LBD16 and LBD18 acting downstream of ARF7 and ARF19 are involved in adventitious root formation in Arabidopsis. Lee, H. W., Cho, C., Pandey, S. K., Park, Y., Kim, M., & Kim, J. BMC Plant Biology, 19(1): 46. January 2019.

LBD16 and LBD18 acting downstream of ARF7 and ARF19 are involved in adventitious root formation in Arabidopsis [link]

Paper doi link bibtex abstract

@article{lee_lbd16_2019,
	title = {{LBD16} and {LBD18} acting downstream of {ARF7} and {ARF19} are involved in adventitious root formation in {Arabidopsis}},
	volume = {19},
	issn = {1471-2229},
	url = {https://doi.org/10.1186/s12870-019-1659-4},
	doi = {10.1186/s12870-019-1659-4},
	abstract = {Adventitious root (AR) formation is a complex genetic trait, which is controlled by various endogenous and environmental cues. Auxin is known to play a central role in AR formation; however, the mechanisms underlying this role are not well understood.},
	number = {1},
	urldate = {2023-11-14},
	journal = {BMC Plant Biology},
	author = {Lee, Han Woo and Cho, Chuloh and Pandey, Shashank K. and Park, Yoona and Kim, Min-Jung and Kim, Jungmook},
	month = jan,
	year = {2019},
	keywords = {Adventitious root formation, Arabidopsis thaliana, Auxin response factor, LBD16, LBD18, Lateral organ boundaries domain},
	pages = {46},
}

2018 (2)

Coiled-coil motif in LBD16 and LBD18 transcription factors are critical for dimerization and biological function in arabidopsis. Pandey, S. K., & Kim, J. Plant Signaling & Behavior, 13(1): e1411450. January 2018. Publisher: Taylor & Francis _eprint: https://doi.org/10.1080/15592324.2017.1411450

Coiled-coil motif in LBD16 and LBD18 transcription factors are critical for dimerization and biological function in arabidopsis [link]

Paper doi link bibtex abstract

@article{pandey_coiled-coil_2018,
	title = {Coiled-coil motif in {LBD16} and {LBD18} transcription factors are critical for dimerization and biological function in arabidopsis},
	volume = {13},
	issn = {null},
	url = {https://doi.org/10.1080/15592324.2017.1411450},
	doi = {10.1080/15592324.2017.1411450},
	abstract = {The LATERAL ORGAN BOUNDARIES (LOB) DOMAIN (LBD) gene family members encode a class of plant-specific transcription factors that play important roles in many different aspects of plant growth and development. The LBD proteins contain a conserved LOB domain harboring a Leu zipper-like coiled-coil motif, which has been predicted to mediate protein-protein interactions among the LBD family members. Dimerization of transcription factors is crucial for the modulation of their DNA-binding affinity, specificity, and diversity, contributing to the transcriptional regulation of distinct cellular and biological responses. Our various molecular and biochemical experiments with genetic approaches on LBD16 and LBD18, which are known to control lateral root development in Arabidopsis, demonstrated that the conserved Leu or Val residues in the coiled-coil motifs of these transcription factors are critical for their dimerization as well as the transcriptional regulation to display their biological functions during lateral root formation. We further showed that beside the coiled-coil motif, the carboxyl-terminal region in LBD18 acts as an additional dimerization domain. These findings provide a molecular framework for the homo- and hetero-dimerization of the LBD family proteins for displaying their distinct and diverse biological functions in plants.},
	number = {1},
	urldate = {2023-11-14},
	journal = {Plant Signaling \& Behavior},
	author = {Pandey, Shashank K. and Kim, Jungmook},
	month = jan,
	year = {2018},
	pmid = {29227192},
	note = {Publisher: Taylor \& Francis
\_eprint: https://doi.org/10.1080/15592324.2017.1411450},
	keywords = {Arabidopsis, LBD16, LBD18, coiled-coil motif, lateral organ boundaries domain, lateral root development, protein-protein interactions, transcriptional regulation},
	pages = {e1411450},
}

LBD18 uses a dual mode of a positive feedback loop to regulate ARF expression and transcriptional activity in Arabidopsis. Pandey, S. K., Lee, H. W., Kim, M., Cho, C., Oh, E., & Kim, J. The Plant Journal, 95(2): 233–251. 2018. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.13945

LBD18 uses a dual mode of a positive feedback loop to regulate ARF expression and transcriptional activity in Arabidopsis [link]

Paper doi link bibtex abstract

@article{pandey_lbd18_2018,
	title = {{LBD18} uses a dual mode of a positive feedback loop to regulate {ARF} expression and transcriptional activity in {Arabidopsis}},
	volume = {95},
	copyright = {© 2018 The Authors The Plant Journal © 2018 John Wiley \& Sons Ltd},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/tpj.13945},
	doi = {10.1111/tpj.13945},
	abstract = {A hierarchy of transcriptional regulators controlling lateral root formation in Arabidopsis thaliana has been identified, including the AUXIN RESPONSE FACTOR 7 (ARF7)/ARF19-LATERAL ORGAN BOUNDARIES DOMAIN 16 (LBD16)/LBD18 transcriptional network; however, their feedback regulation mechanisms are not known. Here we show that LBD18 controls ARF activity using the dual mode of a positive feedback loop. We showed that ARF7 and ARF19 directly bind AuxRE in the LBD18 promoter. A variety of molecular and biochemical experiments demonstrated that LBD18 binds a specific DNA motif in the ARF19 promoter to regulate its expression in vivo as well as in vitro. LBD18 interacts with ARFs including ARF7 and ARF19 via the Phox and Bem1 domain of ARF to enhance the transcriptional activity of ARF7 on AuxRE, and competes with auxin/indole-3-acetic acid (IAA) repressors for ARF binding, overriding the negative feedback loop exerted by Aux/IAA repressors. Taken together, these results show that LBD18 and ARFs form a double positive feedback loop, and that LBD18 uses the dual mode of a positive feedback loop by binding directly to the ARF19 promoter and through the protein–protein interactions with ARF7 and ARF19. This novel mechanism of feedback loops may constitute a robust feedback mechanism that ensures continued lateral root growth in response to auxin in Arabidopsis.},
	language = {en},
	number = {2},
	urldate = {2023-11-14},
	journal = {The Plant Journal},
	author = {Pandey, Shashank K. and Lee, Han Woo and Kim, Min-Jung and Cho, Chuloh and Oh, Eunkyoo and Kim, Jungmook},
	year = {2018},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.13945},
	keywords = {Arabidopsis thaliana, auxin, feedback regulation, lateral root development, protein–protein interaction, transcriptional regulation},
	pages = {233--251},
}

2017 (1)

Dimerization in LBD16 and LBD18 Transcription Factors Is Critical for Lateral Root Formation. Lee, H. W., Kang, N. Y., Pandey, S. K., Cho, C., Lee, S. H., & Kim, J. Plant Physiology, 174(1): 301–311. May 2017.

Dimerization in LBD16 and LBD18 Transcription Factors Is Critical for Lateral Root Formation [link]

Paper doi link bibtex abstract

@article{lee_dimerization_2017,
	title = {Dimerization in {LBD16} and {LBD18} {Transcription} {Factors} {Is} {Critical} for {Lateral} {Root} {Formation}},
	volume = {174},
	issn = {0032-0889},
	url = {https://doi.org/10.1104/pp.17.00013},
	doi = {10.1104/pp.17.00013},
	abstract = {LATERAL ORGAN BOUNDARIES DOMAIN/ASYMMETRIC LEAVES2-LIKEs (hereafter referred to as LBD) are plant-specific transcription factors that play important roles in a plethora of plant growth and development. The leucine (Leu) zipper-like coiled-coil motif in the lateral organ boundaries domain of the class I LBD proteins has been proposed to mediate protein dimerization, but it has not been experimentally assessed yet. LBD16 and LBD18 have been well characterized to play important roles in lateral root development in Arabidopsis (Arabidopsis thaliana). Here, we investigated the role of the coiled-coil motif in the dimerization of LBD16 and LBD18 and in transcriptional regulation and biological function. We built the molecular models of the coiled coil of LBD16 and LBD18, providing the probable Leu zipper models of the helix dimer. Using a variety of molecular techniques, such as bimolecular fluorescence complementation, luciferase complementation imaging, GST pull down, and coimmunoprecipitation assays, we showed that the conserved Leu or valine residues in the coiled-coil motif are critical for the dimerization of LBD16 or LBD18. Using transgenic Arabidopsis plants that overexpress HA:LBD16 or HA:LBD16Q in lbd16 or HA:LBD18 or HA:LBD18Q in lbd18, we demonstrated that the homodimerization of LBD18 mediated by the coiled-coil motif is crucial for transcriptional regulation via promoter binding and for lateral root formation. In addition, we found that the carboxyl-terminal region beyond the coiled-coil motif in LBD18 acts as an additional dimerization domain. These results provide a molecular basis for homodimerization and heterodimerization among the 42 Arabidopsis LBD family members for displaying their biological functions.},
	number = {1},
	urldate = {2023-11-14},
	journal = {Plant Physiology},
	author = {Lee, Han Woo and Kang, Na Young and Pandey, Shashank K. and Cho, Chuloh and Lee, Sung Haeng and Kim, Jungmook},
	month = may,
	year = {2017},
	pages = {301--311},
}

2016 (2)

Expression and Protein Interaction Analyses Reveal Combinatorial Interactions of LBD Transcription Factors During Arabidopsis Pollen Development. Kim, M., Kim, M., Pandey, S., & Kim, J. Plant and Cell Physiology, 57(11): 2291–2299. November 2016.

Paper doi link bibtex abstract

@article{kim_expression_2016,
	title = {Expression and {Protein} {Interaction} {Analyses} {Reveal} {Combinatorial} {Interactions} of {LBD} {Transcription} {Factors} {During} {Arabidopsis} {Pollen} {Development}},
	volume = {57},
	issn = {0032-0781},
	url = {https://doi.org/10.1093/pcp/pcw145},
	doi = {10.1093/pcp/pcw145},
	abstract = {LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factor gene family members play key roles in diverse aspects of plant development. LBD10 and LBD27 have been shown to be essential for pollen development in Arabidopsis thaliana. From the previous RNA sequencing (RNA-Seq) data set of Arabidopsis pollen, we identified the mRNAs of LBD22, LBD25 and LBD36 in addition to LBD10 and LBD27 in Arabidopsis pollen. Here we conducted expression and cellular analysis using GFP:GUS (green fluorescent protein:β-glucuronidase) reporter gene and subcellular localization assays using LBD:GFP fusion proteins expressed under the control of their own promoters in Arabidopsis. We found that these LBD proteins display spatially and temporally distinct and overlapping expression patterns during pollen development. Bimolecular fluorescence complementation and GST (glutathione S-transferase) pull-down assays demonstrated that protein–protein interactions occur among the LBDs exhibiting overlapping expression during pollen development. We further showed that LBD10, LBD22, LBD25, LBD27 and LBD36 interact with each other to form heterodimers, which are localized to the nucleus in Arabidopsis protoplasts. Taken together, these results suggest that combinatorial interactions among LBD proteins may be important for their function in pollen development in Arabidopsis.},
	number = {11},
	urldate = {2023-11-14},
	journal = {Plant and Cell Physiology},
	author = {Kim, Mirim and Kim, Min-Jung and Pandey, Shashank and Kim, Jungmook},
	month = nov,
	year = {2016},
	pages = {2291--2299},
}

Virus-induced gene silencing (VIGS)-mediated functional characterization of two genes involved in lignocellulosic secondary cell wall formation. Pandey, S. K., Nookaraju, A., Fujino, T., Pattathil, S., & Joshi, C. P. Plant Cell Reports, 35(11): 2353–2367. November 2016.

Paper doi link bibtex abstract

@article{pandey_virus-induced_2016,
	title = {Virus-induced gene silencing ({VIGS})-mediated functional characterization of two genes involved in lignocellulosic secondary cell wall formation},
	volume = {35},
	issn = {1432-203X},
	url = {https://doi.org/10.1007/s00299-016-2039-2},
	doi = {10.1007/s00299-016-2039-2},
	abstract = {Functional characterization of two tobacco genes, one involved in xylan synthesis and the other, a positive regulator of secondary cell wall formation, is reported.},
	language = {en},
	number = {11},
	urldate = {2023-11-14},
	journal = {Plant Cell Reports},
	author = {Pandey, Shashank K. and Nookaraju, Akula and Fujino, Takeshi and Pattathil, Sivakumar and Joshi, Chandrashekhar P.},
	month = nov,
	year = {2016},
	keywords = {Bioethanol production, Saccharification, Secondary cell wall (SCW), Transcriptional regulation, Virus-induced gene silencing (VIGS), Xylan synthesis},
	pages = {2353--2367},
}

2014 (1)

Enhanced accumulation of fatty acids and triacylglycerols in transgenic tobacco stems for enhanced bioenergy production. Nookaraju, A., Pandey, S. K., Fujino, T., Kim, J. Y., Suh, M. C., & Joshi, C. P. Plant Cell Reports, 33(7): 1041–1052. July 2014.

Enhanced accumulation of fatty acids and triacylglycerols in transgenic tobacco stems for enhanced bioenergy production [link]

Paper doi link bibtex abstract

@article{nookaraju_enhanced_2014,
	title = {Enhanced accumulation of fatty acids and triacylglycerols in transgenic tobacco stems for enhanced bioenergy production},
	volume = {33},
	issn = {1432-203X},
	url = {https://doi.org/10.1007/s00299-014-1582-y},
	doi = {10.1007/s00299-014-1582-y},
	abstract = {We report a novel approach for enhanced accumulation of fatty acids and triacylglycerols for utilization as biodiesel in transgenic tobacco stems through xylem-specific expression ofArabidopsis DGAT1andLEC2genes.},
	language = {en},
	number = {7},
	urldate = {2023-11-14},
	journal = {Plant Cell Reports},
	author = {Nookaraju, Akula and Pandey, Shashank K. and Fujino, Takeshi and Kim, Ju Young and Suh, Mi Chung and Joshi, Chandrashekhar P.},
	month = jul,
	year = {2014},
	keywords = {Biodiesel, Renewable energy, Tobacco, Triacylglycerols, Xylem},
	pages = {1041--1052},
}

2013 (1)

Designing Cell Walls for Improved Bioenergy Production. Nookaraju, A., Pandey, S. K., Bae, H., & Joshi, C. P. Molecular Plant, 6(1): 8–10. January 2013.

Designing Cell Walls for Improved Bioenergy Production [link]

Paper doi link bibtex

@article{nookaraju_designing_2013,
	title = {Designing {Cell} {Walls} for {Improved} {Bioenergy} {Production}},
	volume = {6},
	issn = {1674-2052},
	url = {https://www.sciencedirect.com/science/article/pii/S1674205214608741},
	doi = {10.1093/mp/sss111},
	number = {1},
	urldate = {2023-11-14},
	journal = {Molecular Plant},
	author = {Nookaraju, Akula and Pandey, Shashank K. and Bae, Hyeun-Jong and Joshi, Chandrashekhar P.},
	month = jan,
	year = {2013},
	pages = {8--10},
}

2012 (2)

Plant disease resistance genes: Current status and future directions. Gururani, M. A., Venkatesh, J., Upadhyaya, C. P., Nookaraju, A., Pandey, S. K., & Park, S. W. Physiological and Molecular Plant Pathology, 78: 51–65. April 2012.

Plant disease resistance genes: Current status and future directions [link]

Paper doi link bibtex abstract

@article{gururani_plant_2012,
	title = {Plant disease resistance genes: {Current} status and future directions},
	volume = {78},
	issn = {0885-5765},
	shorttitle = {Plant disease resistance genes},
	url = {https://www.sciencedirect.com/science/article/pii/S0885576512000033},
	doi = {10.1016/j.pmpp.2012.01.002},
	abstract = {Plant diseases can drastically abate the crop yields as the degree of disease outbreak is getting severe around the world. Therefore, plant disease management has always been one of the main objectives of any crop improvement program. Plant disease resistance (R) genes have the ability to detect a pathogen attack and facilitate a counter attack against the pathogen. Numerous plant R-genes have been used with varying degree of success in crop improvement programs in the past and many of them are being continuously exploited. With the onset of recent genomic, bioinformatics and molecular biology techniques, it is quite possible to tame the R-genes for efficiently controlling the plant diseases caused by pathogens. This review summarizes the recent applications and future potential of R-genes in crop disease management.},
	urldate = {2023-11-14},
	journal = {Physiological and Molecular Plant Pathology},
	author = {Gururani, Mayank Anand and Venkatesh, Jelli and Upadhyaya, Chandrama Prakash and Nookaraju, Akula and Pandey, Shashank Kumar and Park, Se Won},
	month = apr,
	year = {2012},
	keywords = {Disease management, Plant diseases, Plant pathogens, Resistance genes},
	pages = {51--65},
}

Role of Ca2+-mediated signaling in potato tuberization: An overview. Nookaraju, A., Pandey, S., Upadhyaya, C., Heung, J. J., Kim, H. S, Chun, S. C., Kim, D. H., & Park, S. W. Botanical Studies, 53: 177–189. 2012.

Role of Ca2+-mediated signaling in potato tuberization: An overview [link]

Paper link bibtex abstract

@article{nookaraju_role_2012,
	title = {Role of {Ca2}+-mediated signaling in potato tuberization: {An} overview},
	volume = {53},
	url = {https://ejournal.sinica.edu.tw/bbas/content/2012/2/Bot532-01/Bot532-01.html},
	abstract = {Potato tuberization represents the morphogenetic transition of underground shoot to tuber involving several biochemical and molecular changes under complex environmental, nutritional and endogenous regulation. Among the nutritional factors, the role of calcium in potato tuberization is documented in several earlier studies. Calcium is a major essential nutrient required for normal growth and development of plants. As a second messenger it plays a role in a number of fundamental cellular processes like cytoplasmic streaming, thigmotropism, gravitropism, cell division, cell differentiation, photomorphogenesis, plant defense and various stress responses. Calcium in the cytosol regulates the activity of Ca2+-sensor proteins and these proteins will subsequently activate and/or modify the activity of target proteins in biological pathways. Also, cytosolic calcium regulates oxidative burst via calcium dependent protein kinases (CDPKs) and induces many intracellular signaling pathways. Studies suggest that Ca2+ and Ca2+-sensor protein calmodulin (CaM) have a role as signal molecules for tuber induction in potato. Also, a potato Ca2+-dependent protein kinase, StCDPK1, is reported to be transiently expressed in tuberizing stolons suggesting its possible involvement in potato tuberization by transcriptional activation of some of the tuberizing genes. Though Ca2+ and Ca2+-regulated proteins influence many developmental processes in plants, the exact molecular and biochemical mechanism of Ca2+-mediated signal pathways controlling potato tuberization is still not clear. This review sheds some light on the possible molecular mechanisms involved in the Ca2+-mediated signaling in potato tuberization.},
	urldate = {2023-11-14},
	journal = {Botanical Studies},
	author = {Nookaraju, Akula and Pandey, Shashank and Upadhyaya, Chandrama and Heung, Jeon Jae and Kim, Hyun S and Chun, Se Chul and Kim, Doo Hwan and Park, Se Won},
	year = {2012},
	keywords = {⛔ No DOI found},
	pages = {177--189},
}

2011 (1)

An Update on Biotechnological Approaches for Improving Abiotic Stress Tolerance in Tomato. Pandey, S. K., Nookaraju, A., Upadhyaya, C. P., Gururani, M. A., Venkatesh, J., Kim, D., & Park, S. W. Crop Science, 51(6): 2303–2324. 2011. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.2135/cropsci2010.10.0579

An Update on Biotechnological Approaches for Improving Abiotic Stress Tolerance in Tomato [link]

Paper doi link bibtex abstract

@article{pandey_update_2011,
	title = {An {Update} on {Biotechnological} {Approaches} for {Improving} {Abiotic} {Stress} {Tolerance} in {Tomato}},
	volume = {51},
	copyright = {Copyright © by the Crop Science Society of America, Inc.},
	issn = {1435-0653},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.2135/cropsci2010.10.0579},
	doi = {10.2135/cropsci2010.10.0579},
	abstract = {Tomato (Solanum lycopersicum L.) is the second most important vegetable crop in the world after potato (Solanum tuberosum L.), and its productivity is influenced by different abiotic stresses. Though cultivated tomato is moderately tolerant to various abiotic stresses, the crop losses due to unfavorable environmental conditions can be unpredictably severe. So far, several efforts have been made to improve abiotic stress tolerance in cultivated tomato through cultural practices, breeding techniques, and biotechnological approaches. Introgression of abiotic stress tolerance to cultivated tomato from more tolerant wild relatives through classical breeding has been attempted with limited success. However, genetic engineering based on the introgression of genes that are known to be involved in stress response and putative stress tolerance could provide powerful tools for improving abiotic stress tolerance in tomato coupled with the growing knowledge of stress physiology. The present review summarizes the current status and future directions on the use of biotechnological approaches to improve abiotic stress tolerance in tomato.},
	language = {en},
	number = {6},
	urldate = {2023-11-14},
	journal = {Crop Science},
	author = {Pandey, Shashank K. and Nookaraju, Akula and Upadhyaya, Chandrama P. and Gururani, Mayank A. and Venkatesh, Jelli and Kim, Doo-Hwan and Park, Se Won},
	year = {2011},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.2135/cropsci2010.10.0579},
	pages = {2303--2324},
}

2010 (1)

Molecular approaches for enhancing sweetness in fruits and vegetables. Nookaraju, A., Upadhyaya, C. P., Pandey, S. K., Young, K. E., Hong, S. J., Park, S. K., & Park, S. W. Scientia Horticulturae, 127(1): 1–15. November 2010.

Molecular approaches for enhancing sweetness in fruits and vegetables [link]

Paper doi link bibtex abstract

@article{nookaraju_molecular_2010,
	title = {Molecular approaches for enhancing sweetness in fruits and vegetables},
	volume = {127},
	issn = {0304-4238},
	url = {https://www.sciencedirect.com/science/article/pii/S030442381000422X},
	doi = {10.1016/j.scienta.2010.09.014},
	abstract = {The quality of fruits and vegetables is mainly dependant on the sweetness determined by the level of soluble sugars such as glucose, fructose and sucrose. Other fruit quality parameters include Brix content, acidity, aroma, color, size and shape. Total sugar content in fruits and vegetables is a function of genetic, nutritional, environmental and developmental factors. Understanding the factors controlling sweetness is important to design strategies for enhancing quality of fruits and vegetables. Modifying the activity of enzymes in carbohydrate metabolism such as sucrose synthase (SuSy), acid invertase, ADP-glucose pyrophosphorylase (AGPase), sucrose phosphate synthase (SPS) and sucrose transporters were found to influence carbohydrate partitioning and sucrose accumulation in sink tissues of several food crops. Plant based taste-modifying sweet proteins such as brazzein, cucurmin, mabinlin, monellin, miraculin, neoculin and thaumatin have potential application for developing transgenic plants to improve the sweetness and quality of fruits and vegetables. The present review envisages various cultural, breeding and molecular approaches used for enhancing sugar content and sweetness in fruits and vegetables.},
	number = {1},
	urldate = {2023-11-14},
	journal = {Scientia Horticulturae},
	author = {Nookaraju, Akula and Upadhyaya, Chandrama P. and Pandey, Shashank K. and Young, Ko Eun and Hong, Se Jin and Park, Suk Keun and Park, Se Won},
	month = nov,
	year = {2010},
	keywords = {Carbohydrate partitioning, Flavor, Metabolic engineering, Sucrose, Sweet proteins},
	pages = {1--15},
}

Pandey, Shashank - Decoding the molecular control of bud dormancy release in trees

Research

Elucidating the role of AGL8-mediated FT1 activation in inducing the release of bud dormancy

Determination of AGL8’s role in hormonal control of bud dormancy release in response to temperature cues

Uncovering the role of AGL8-regulated PD opening in bud dormancy release

CV S. K. Pandey

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