Ph.D. Cellular and Developmental Biology Harvard University, 1991
Luan Laboratory studies how plants perceive and respond to extracellular signals through modifying their developmental and physiological programs. Studies in Luan Lab have identified a new molecular network for calcium signal transduction in plants. Downstream of these early signaling events, plants respond and adapt to environmental changes by regulating the biochemical processes including those at the plasma membrane, vacuolar membrane, and in the chloroplasts.
Signal Transduction and Chloroplast Biology
Environmental Sensing through the CBL-CIPK Ca2+ Signaling Network
CBL-CIPK in nutrient sensing: Plants are growing in a nutrient-poor environment especially after a long history of farming. Agricultural production is heavily relying on the application of chemical fertilizers, opposing a serious economic and environmental problem worldwide. One solution would be to breed crops that can tolerate low-nutrient soils without the need of fertilizers. Recent work in Luan laboratory identified a CBL-CIPK signaling pathway that regulates the activity of a voltage-gated potassium channels involved in K-uptake in plant roots. Manipulation of CBL-CIPK network can therefore enhance the growth of plants under low-K soils, impacting agriculture and environment. (See Li et al., 2006 to get started on this subject). Furthermore, CBL-CIPK network also regulates nutrient homeostasis through targeting transport processes across the tonoplast (vacuolar membrane). This mechanism is exemplified by high Mg-detoxification mediated by multiple CBL-CIPK complexes associated with tonoplast (Tang et al., 2012; 2015).
CBL-CIPK in stress and ABA responses:Several CBL-CIPK pathways have been identified that function in plant responses to environmental stress conditions including salt, drought, and cold. CBL-CIPK network is also involved in the response to plant hormones such as ABA that regulates stress responses. The crosstalk and interaction among the CBLs and CIPKs form a complex signaling network that links environmental responses to biochemical processes in plant cells. (See Cheong et al., 2003 and Pandey et al., 2004 to get started on this subject).
Energy Conversion and Metabolic Regulation in Chloroplasts
After environmental signals are perceived and interpreted by signaling pathways, plant cells respond to the signals by biochemical and physiological changes downstream of the signaling process. Many of the biochemical changes in plants involve metabolic processes in the chloroplasts that serve as a critical “factory” for plant productivity. The best known photosynthetic process include both light harvesting by the photosystems and carbon fixation. As the most important metabolic process, photosynthetic activity and its regulation are connected to all environmental changes. Although the basic biochemical pathways are largely known, the regulatory pathways that link the environmental signals to the light and dark reactions are poorly understood. Luan laboratory focus on the mechanisms underlying regulation of photosynthetic activity by environmental signals.
Light reaction and bio-energy conversion: We are interested in the mechanism of assembly and maintenance of the photosystems that harvest light energy and convert it into the chemical forms. Our recent studies have discovered a family of protein foldases and chaperones (called immunophilins) in the chloroplast that function in the assembly and maintenance of photosynthetic electron transport complexes. Because maintaining the function of photosynthetic complexes is one of the limiting factors in photosynthetic activity, our findings on the immunophilins in the chloroplast will provide information for enhancing light energy conversion by plants.This project has been a collaboration with Prof. Bob B. Buchanan (See Lima et al., 2006; Fu et al., 2007; Che et al., 2013; Hou et al., 2015 to get started on this subject).
Dark Reaction and Biomass: The output of photosynthetic carbon fixation is transitory starch in the chloroplast. The starch biosynthesis and degradation is under tight control by environmental factors such as light-dark cycle and stress conditions. Although regulation of glycogen (starch) metabolism is well understood in animal cells, our understanding of metabolic regulation of starch accumulation is still in its infancy. Recent research in Luan laboratory identified a protein phosphatase (DSP4) that plays a central role in regulating starch accumulation in Arabidopsis chloroplasts, providing a strong evidence that protein phosphorylation is involved in starch regulation. In addition, the DSP4 activity is regulated by redox states that are controlled by light-dark transition. Therefore DSP4 may provide a molecular link between diurnal cycle and starch accumulation. As starch is one of the most abundant plant-derived polymers, its sheer biomass and ease of production make it a critical source for biofuel production. Understanding the regulatory mechanism for starch accumulation in plants will directly impact the biomass production and biofuel industry.(See Sokolov et al., 2006 to get started on this subject).
Zhang H, Zhao FG, Tang RJ, Yu Y, Song J, Wang Y, Li L, Luan S. (2017) Two tonoplast MATE proteins function as turgor-regulating chloride channels in <i>Arabidopsis</i>. Proc Natl Acad Sci U S A. 2017 Feb 15. pii: 201616203. doi: 10.1073/pnas.1616203114.
Du C, Li X, Chen J, Chen W, Li B, Li C, Wang L, Li J, Zhao X, Lin J, Liu X, Luan S, Yu F. (2016) Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc Natl Acad Sci U S A. 2016 Dec 20;113(51):E8326-E8334.
Chen J, Yu F, Liu Y, Du C, Li X, Zhu S, Wang X, Lan W, Rodriguez PL, Liu X, Li D, Chen L, Luan S. (2016) FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):E5519-27. doi: 10.1073/pnas.1608449113.
Liu J, Yang L, Luan M, Wang Y, Zhang C, Zhang B, Shi J, Zhao FG, Lan W, Luan S. (2015) A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proc Natl Acad Sci U S A. 2015 Nov 24;112(47):E6571-8.
Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX, Luan S. (2015) Tonoplast CBL-CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad Sci U S A. 112(10):3134-9.
Hou X, Fu A, Garcia VJ, Buchanan BB, Luan S. (2015) PSB27: A thylakoid protein enabling Arabidopsis to adapt to changing light intensity. Proc Natl Acad Sci U S A. 112(5):1613-8.
Tian W, Hou C, Ren Z, Pan Y, Jia J, Zhang H, Bai F, Zhang P, Zhu H, He Y, Luo S, Li L, Luan S. (2015) A molecular pathway for CO₂ response in Arabidopsis guard cells. Nat Commun. 20;6:6057. doi: 10.1038/ncomms7057.
Maierhofer T, Diekmann M, Offenborn JN, Lind C, Bauer H, Hashimoto K, S Al-Rasheid KA, Luan S, Kudla J, Geiger D, Hedrich R. (2014) Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci Signal. 9;7(342):ra86.
Mao D, Chen J, Tian L, Liu Z, Yang L, Tang R, Li J, Lu C, Yang Y, Shi J, Chen L, Li D, Luan S (2014) Arabidopsis Transporter MGT6 Mediates Magnesium Uptake and Is Required for Growth under Magnesium Limitation. Plant Cell 26(5):2234-2248.
Hou C, Tian W, Kleist T, He K, Garcia V, Bai F, Hao Y, Luan S, Li L (2014) DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res. 24(5):632-5.
Zhou L, Lan W, Jiang Y, Fang W, Luan S (2014) A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol Plant. 7(2):369-76.
Che Y, Fu A, Hou X, McDonald K, Buchanan BB, Huang W, Luan S (2013) C-terminal processing of reaction center protein D1 is essential for the function and assembly of photosystem II in Arabidopsis. Proc Natl Acad Sci U S A. 110(40):16247-52.
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci U S A. 110(38):15485-90.
Park SW, Li W, Viehhauser A, He B, Kim S, Nilsson AK, Andersson MX, Kittle JD, Ambavaram MM, Luan S, Esker AR, Tholl D, Cimini D, Ellerström M, Coaker G, Mitchell TK, Pereira A, Dietz KJ, Lawrence CB (2013) Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc Natl Acad Sci U S A. 110(23):9559-64.
Lee SC, Lim CW, Lan W, He K, Luan S. (2013) ABA signaling in guard cells entails a dynamic protein-protein interaction relay from the PYL-RCAR family receptors to ion channels. Mol Plant. 6(2):528-38.
Tang RJ, Liu H, Yang Y, Yang L, Gao XS, Garcia VJ, Luan S, Zhang HX (2012) Tonoplast calcium sensors CBL2 and CBL3 control plant growth and ion homeostasis through regulating V-ATPase activity in Arabidopsis. Cell Res. 2012 Dec;22(12):1650-65.
Yu F, Qian L, Nibau C, Duan Q, Kita D, Levasseur K, Li X, Lu C, Li H, Hou C, Li L, Buchanan BB, Chen L, Cheung AY, Li D, Luan S. (2012) FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci U S A. 109(36):14693-8.
Meng L, Buchanan BB, Feldman LJ, Luan S. (2012) CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc Natl Acad Sci U S A. 109, 1760-5.
Batistic, O., Kim, K-N., Kleist, T., Kudla, J., Luan, S. (2011) The CBL-CIPK signaling network in plants. Book Chapter in “Coding and Decoding of Calcium Signals in Plants”. Edited by S. Luan, Springer Publishing Inc.
Li H, Luan S. (2010) P53 is a histone chaperone required for repression of ribosomal RNA gene expression in Arabidopsis. Cell Res. 20, 357-66.
Lan, W., Wang, W., Buchanan, BB. and Luan, S. (2010) A Rice HKT-type transporter conceals a calcium-permeable cation channel. Proc. Natl. Acad. Sci. USA. 107, 7089-94.
Yu F, Shi J, Zhou J, Gu J, Chen Q, Li J, Cheng W, Mao D, Tian L, Buchanan BB, Li L, Chen L, Li D, Luan S. (2010) ANK6, a mitochondrial ankyrin repeat protein, is required for male-female gamete recognition in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 107, 22332-7.
Wu, W-H., Wang, Y., Lee, S.C., Lan, W., Luan, S. (2010) Regulation of ion channels by the calcium signaling network in plant cells. Book Chapter in “Ion Channels and Plant Stress Responses” Book edited by V. Demidchik and F. Maathuis; Springer Publishing Inc.
Chae, L., Cheong, Y., Kim, K., Pandey, G., Luan, S. (2010) Protein kinases and phosphatases in abiotic stress responses in plants. Book Chapter in “Abiotic Stress Adaptation in Plants” Book edited by Pareek, et al. Springer Publishing Inc.
Sun SY, Chao DY, Li XM, Shi M, Gao JP, Zhu MZ, Yang HQ, Luan S, Lin HX (2009) OsHAL3 mediates a new pathway in the light-regulated growth of rice. Nat Cell Biol. 11, 845-51.
Luan, S. (2009) The CBL-CIPK network in plant calcium signaling. Trends in Plant Sci. 14(1):37-42.
Luan, S., Lan, W., and S-C, Lee (2009) Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network. Curr. Opin. Plant Biol. 12, 339-346.
Lee, S., Lan, W., Buchanan, BB, Luan, S. (2009) Protein kinase and phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl. Acad. Sci. USA. 106, 21419-24.
Luan, S. (2008) Paradigms and networks for intracellular calcium signaling in plants. Book Chapter in Annual Plant Reviews, vol 33 “Intracellular Signaling in Plants”. Ed. Z. Yang, Wiley-Blackwell.
Dominguez-Solis JR, He Z, Lima A, Ting J, Buchanan BB, Luan S. (2008) A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc Natl Acad Sci U S A. 105(42):16386-91. Epub 2008 Oct 9. Abstract
Li L, Liu K, Hu Y, Li D, Luan S. (2008) Single mutations convert an outward K+ channel into an inward K+ channel. Proc Natl Acad Sci U S A. 105(8):2871-6. Epub 2008 Feb 19. Abstract
Chen X, Lin WH, Wang Y, Luan S, Xue HW. (2008) An inositol polyphosphate 5-phosphatase functions in PHOTOTROPIN1 signaling in Arabidopis by altering cytosolic Ca2+. Plant Cell 20(2):353-66. Epub 2008 Feb 5. Abstract
Li H, He Z, Lu G, Lee SC, Alonso J, Ecker JR, Luan, S. (2007) A WD40 Domain Cyclophilin Interacts with Histone H3 and Functions in Gene Repression and Organogenesis in Arabidopsis. Plant Cell. 19, 2403-2416.
Pandey GK, Cheong YH, Kim BG, Grant JJ, Li L, Luan, S. (2007) CIPK9: a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis. Cell Res. 17, 411-421. Abstract
Fu A, He Z, Cho HS, Lima A, Buchanan BB, Luan S. (2007) A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 104, 15947-15952. Abstract
Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S. (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 52, 223-239. Abstract
Lee SC, Lan WZ, Kim BG, Li L, Cheong YH, Pandey GK, Lu G, Buchanan BB, Luan S. (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci U S A. 104, 15959-15964. Abstract
Liu, K., Li, L., Luan, S. (2006) Intracellular potassium sensing of SKOR, a shaker-type K-channel from Arabidopsis. Plant J. 46, 260-268.
Sokolov, L., Allery, A., Buchanan, B.B., and Luan, S. (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc. Natl. Acad. Sci. USA. 103, 9732-9737.
Li, L., Kim, B., Cheong, Y., Pandey, G., and Luan, S. (2006) A calcium signaling pathway regulates a potassium channel for low-potassium response in Arabidopsis. Proc. Natl. Acad. Sci. USA. 103:12625-30.
Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S. (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 103:12631-6.
Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S*, Lin HX*. (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genetics 37, 1141-1146. (News and Views on page 1029-1030, *corresponding author).
Romano P, Gray J, Horton P, Luan S. (2005) Plant immunophilins: functional versatility beyond protein maturation. (Tanksley Review) New Phytol. 166, 753-69.
Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Heroux A, Buchanan BB, Swaminathan K, Luan S. (2004) Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci U S A. 101, 13945-50.
Pandey, G., Cheong, Y., Kim, N., Luan, S. (2004) Calcium sensor calcineurin B-like 9 modulates sensitivityand biosynthesis of ABA in Arabidopsis. Plant Cell 16, 1912-1924.
Kim, K., Cheong, Y., Grant, J., Pandey, G., and Luan, S. (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15, 411-423.
Luan, S. (2003) Protein phosphatases in plants. Annu. Rev. Plant Biol. 54, 69-90.
Kim, K., Cheong, Y., Grant, J., Pandey, G., and Luan, S. (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15, 411-423. [Abstract | PDF]
Cheong, Y., Kim, K., Pandey, G.K., Gupta, R., Grant, J., and Luan, S. (2003) CBL1, a Calcium Sensor That Differentially Regulates Salt, Drought, and Cold Responses in Arabidopsis. Plant Cell 15, 1833-1845. [Abstract | PDF]
Gupta, R., Mould, R., and Luan, S. (2002) A chloroplast FKBP interact and regulates the accumulation of Rieske subunit of cytochrome b/f complex in photosynthetic electron transport. Proc. Natl. Acad. Sci. USA 99, 15806-15811. [Abstract | PDF]
Gupta, R., Ting, T., Sokolov, L., Johnson, S.J., and Luan, S. (2002) AtPTEN1, a tumor suppressor homologue essential for pollen development in Arabidopsis. Plant Cell 14, 2495--2507. [Abstract | PDF]
Gupta, R., He, Z., and Luan, S. (2002) Functional relationship of cytochrome c6 and plastocyanin in Arabidopsis. Nature 417, 567-571. [Abstract | PDF]
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang H, Eulgem T, Mauch F, Luan S, et al. and Zhu T. (2002). Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses. Plant Cell 14, 559-574. [Abstract | PDF | Supplemental data]
Li L, Tutone AF, Drummond RS, Gardner RC, and Luan S. (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13, 2761-2775. [Abstract | PDF]
Liu, K., and Luan, S. (2001) Internal Aluminum Block of Plant Inward K+ Channels. Plant Cell 13, 1453-1465.[PDF]
Shi, J., Kim, N., Gupta, R., Luan, S.*, and Kudla, J. (1999) Novel protein kinases as common targets for Arabidopsis calcineurin B-like Ca2+ sensors. Plant Cell 11, 2393-2406. *corresponding author
Kudla, J., Xu, Q., Harter, K., Gruissem, W. and Luan, S. (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA 96, 4718-4723. (Accompanied by a PNAS Editorial Commentary: How Plants Learn. PNAS 96, 4216-4218).
Liu, K. and Luan, S. (1998) Voltage-dependent K+ channels as targets for osmosensing in guard cells. Plant Cell 10, 1957-1970.
Xu, Q., Fu, H., Gupta, R. and Luan, S. (1998) Characterization of a protein tyrosine phosphatase encoded by a stress-responsive gene in Arabidopsis . Plant Cell 10, 849-858.
Fu, H. and Luan, S. (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. Plant Cell 10, 63-73.
Luan, S.*, Kudla, J., Gruissem, W. and Schreiber, S.L. (1996) Molecular characterization of a FKBP-type immunophilin from higher plants. Proc. Natl. Acad. Sci. USA 93, 6964-6969. *corresponding author
Luan, S., and Schreiber, S.L. (1994) pCyP B: a chloroplast-localized, heat shockresponsive cyclophilin from fava bean. Plant Cell 6, 885-892.
Luan, S., Albers, M.W., and Schreiber, S.L. (1994) Light-regulated, tissue-specific immunophilins in a higher plant. Proc. Natl. Acad. Sci. USA 91, 984-988.
Luan, S., Li, W., Rusnak, F., Assmann, S.M. and Schreiber, S.L. (1993) Immunosuppressants implicate protein phosphatase-regulation of K+ channels in guard cells. Proc. Natl. Acad. Sci. USA 90, 2202-2206. (Accompanied by a PNAS Editorial Commentary PNAS 90, 3125-3126).
150L - Laboratory for Plant Cell Biology
150 - Plant Cell Biology
H196 - Honors Research
200D - Plant Cell Biology
299 - Graduate Research
Honors & Awards
Highly Cited Researcher (Plant and Animal Sciences, 2014, 2015) Thomson Reuters