Publications

2018
Shor E, Kurtz A, Poltavskaya R, Paik I, Huq E, Green R. PIF-mediated sucrose regulation of the circadian oscillator is light quality and temperature dependent. Genes [Internet]. 9 (12) :628. Publisher's Version
Pham VN, Xu X, Huq E. Molecular bases for the constitutive photomorphogenic phenotypes in Arabidopsis. Development. 145 (23) :dev169870.
Zhao X, Jiang Y, Li J, Huq E, Chen ZJ, Xu D, Deng XW. COP1 SUPPRESSOR 4 promotes seedling photomorphogenesis by repressing CCA1 and PIF4 expression in Arabidopsis. Proc Natl Acad Sci, USA [Internet]. 115 :11631-11636. Publisher's Version
Pham VN, Kathare PK, Huq E. Dynamic regulation of PIF5 by COP1-SPA complex to optimize photomorphogenesis in Arabidopsis. Plant Journal [Internet]. 96 (2) :260-273. Publisher's Version
Song Q, Ando A, Xu D, Fang L, Zhang T, Huq E, Qiao H, Deng XW, Chen ZJ. Diurnal downregulation of ethylene biosynthesis mediates biomass heterosis. PNAS [Internet]. 115 :5606-5611. Publisher's Version
Majee M, Kumar S, Kathare PK, Wu S, Gingerich D, Nayak NR, Salaita L, Dinkins R, Martin K, Goodin M, et al. KELCH F-BOX Protein Positively Influences Seed Germination by Targeting PHYTOCHROME-INTERACTING FACTOR1. PNAS. 115 (17) :E4120-4129.
Huq E. Direct convergence of light and auxin signaling pathways in Arabidopsis. Mol. Plant. 11 (4) :515-517.
Pham VN, Kathare PK, Huq E. Phytochromes and Phytochrome Interacting Factors. Plant Physiology [Internet]. 176 :1025-1038. Publisher's Version
2017
Enderle B, Sheerin DJ, Paik I, Kathare PK, Schwenk P, Klose C, Ulbrich M, Huq E, Hiltbrunner A. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nature Communications. 8 :2221.
Paik I, Kathare PK, Kim J-I, Huq E. Expanding Roles of PIFs in Signal Integration from Multiple Processes. Mol Plant [Internet]. 10 (8) :1035-1046. Publisher's Version
Xin R, Zhu L, Salomé PA, Mancini E, Marshall C, Harmon FG, Yanovsky MJ, Weigel D, Huq E. SPF45-related SPLICING FACTOR FOR PHYTOCHROME SIGNALING promotes photomorphogenesis by regulating pre-mRNA splicing in Arabidopsis. PNAS [Internet]. 114 (33) :E7018-E7027. Publisher's Version
Xu X, Kathare PK, Pham VN, Nguyen A, Bu Q, Huq E. Reciprocal proteasome-mediated degradation of PIFs and HFR1 underlies photomorphogenic development in Arabidopsis. Development [Internet]. 144 (10) :1831-1840. Publisher's Version
Shor E, Paik I, Kangisser S, Green R, Huq E. Phytochrome interacting factors (PIFs) mediate metabolic regulation of the circadian system in Arabidopsis. New Phytologist. 215 (1) :217-228.
Possart A, Xu T, Paik I, Hanke S, Keim S, Hermann H-M, Wolf L, Hiss M, Becker C, Huq E, et al. Characterization of PIFs from the moss Physcomitrella patens illustrates conservation of phytochrome signaling modules in land plants. Plant Cell. 29 :310-330.
2016
Zhu L, Xin R, Huq E. A Protein-Based Genetic Screening Uncovers Mutants Involved in Phytochrome Signaling in Arabidopsis. Front. Plant Sci. 7 :1086.
Zhu L, Xin R, Bu Q, Shen H, Dang J, Huq E. A negative feedback loop between PHYTOCHROME INTERACTING FACTORs and HECATE proteins fine tunes photomorphogenesis in Arabidopsis. The Plant Cell [Internet]. 28 (4) :855-874. Publisher's VersionAbstract

The Phytochrome Interacting Factors (PIFs), a small group of basic helix-loop-helix (bHLH) transcription factors, repress photomorphogenesis both in the dark and light. Light signals perceived by the phytochrome family of photoreceptors induce rapid degradation of PIFs to promote photomorphogenesis. Here we show that HECATE (HEC) proteins, another small group of HLH proteins, antagonistically regulate PIFs to promote photomorphogenesis. HEC1 and HEC2 heterodimerize with PIF family members. PIF1, HEC1 and HEC2 genes are spatially and temporally co-expressed, and HEC2 is localized in the nucleus. hec1, hec2 and hec3 single and hec1 hec2 double mutants showed hyposensitivity to light-induced seed germination, accumulation of chlorophyll and carotenoids, hallmark processes oppositely regulated by PIF1. HEC2 inhibits PIF1 target gene expression by directly heterodimerizing with PIF1 and preventing DNA binding and transcriptional activation activity of PIF1. Conversely, PIFs directly activate the expression of HEC1 and HEC2 in the dark and light reduces the expression of these HECs possibly by degrading PIFs. HEC2 is partially degraded in the dark through the ubiquitin/26S-proteasome pathway and is stabilized by light. HEC2 overexpression also reduces the light-induced degradation of PIF1. Taken together, these data suggest that PIFs and HECs constitute a negative feedback loop to fine tune photomorphogenesis in Arabidopsis thaliana.

Sharma N, Xin R, Kim D-H, Sung S, Lange T, Huq E. NO FLOWERING IN SHORT DAY (NFL) is a bHLH transcription factor thatpromotes flowering specifically under short-day conditions in Arabidopsis. Development [Internet]. 143 (4) : 682-690. Publisher's Version
2015
Xu X, Paik I, Zhu L, Huq E. Illuminating progress in phytochrome-mediated light signaling pathways. Trends in Plant Science. 20 (10) :641-650.Abstract

Light signals regulate a plethora of plant responses throughout their life cycle, especially the red and far-red regions of the light spectrum perceived by the phytochrome family of photoreceptors. However, the mechanisms by which phytochromes regulate gene expression and downstream responses remain elusive. Several recent studies have unraveled the details on how phytochromes regulate photomorphogenesis. These include the identification of E3 ligases
that degrade PHYTOCHROME INTERACTING FACTOR (PIF) proteins, key negative regulators, in response to light, a better view of how phytochromes inhibit another key negative regulator, CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), and an understanding of why plants evolved multiple negative regulators to repress photomorphogenesis in darkness. These advances will surely fuel future research on many unanswered questions that have intrigued plant photobiologists for decades.

Zhu L, Bu Q, Xu X, Paik I, Hunag X, Hoecker U, Deng XW, Huq E. CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1. Nature Communications. 6 :7245.Abstract

Plants undergo contrasting developmental programs in dark and light. Photomorphogenesis, a light-adapted programme is repressed in the dark by the synergistic actions of CUL4COP1–SPA E3 ubiquitin ligase and a subset of basic helix-loop-helix transcription factors called phytochrome interacting factors (PIFs). To promote photomorphogenesis, light activates the phytochrome family of sensory photoreceptors, which inhibits these repressors by poorly understood mechanisms. Here, we show that the CUL4COP1–SPA E3 ubiquitin ligase is necessary for the light-induced degradation of PIF1 in Arabidopsis. The light-induced ubiquitylation and subsequent degradation of PIF1 is reduced in the cop1, spaQ and cul4 backgrounds. COP1, SPA1 and CUL4 preferentially form complexes with the phosphorylated forms of PIF1 in response to light. The cop1 and spaQ seeds display strong hyposensitive response to far-red light-mediated seed germination and light-regulated gene expression. These data show a mechanism by which an E3 ligase attenuates its activity by degrading its cofactor in response to light.

Mulekar JJ, Huq E. Arabidopsis Casein Kinase 2 α4 subunit regulates various developmental pathways in a functionally overlapping manner. Plant Science. 236 :295-303.Abstract

Casein kinase 2 (CK2) is an essential and well-conserved Ser/Thr kinase that regulates proteins in a post-translational manner. CK2 has been shown to affect a large number of developmental processes acrosseukaryotes. It is a tetrameric protein composed of a dimer of alpha (catalytic) and beta (regulatory)subunit each. In our previous study we showed that three of the four CK2 subunits in Arabidopsisact in a functionally redundant manner to regulate various developmental pathways. In this study weconstructed two independent CK2 4 RNAi lines in the CK2 alpha triple mutant background. Throughfunctional characterization of these RNAi lines we show that the fourth subunit in Arabidopsis alsofunctions redundantly in regulating ABA response, lateral root formation and flowering time. CK2 4-GFP localizes to the chloroplast in transgenic Arabidopsis seedlings, consistent with the presence of achloroplast localization signal at the amino-terminus of CK2 4 subunit. Taken together, our results sug-gest a functionally overlapping role for the CK2 4 subunit in regulating various developmental processesin plants

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