People

Research and Teaching

Understanding and improving photosynthesis

My long-term research goals are to understand how photosynthetic energy conversion works, how it is regulated, and how it might be improved to help meet the world’s needs for food and fuel. We use a wide array of experimental organisms and interdisciplinary approaches to investigate fundamental questions about assembly, regulation, and dynamics of photosynthesis. Current lab members study the biosynthesis and function of photosynthetic pigments, assembly and repair of photosynthetic reaction centers, structure and dynamics of the photosynthetic membrane, mechanisms involved in sensing excess light, singlet oxygen signaling, transcriptional regulation of photosynthesis and photoprotection by light and carbon, and regulation of photosynthetic light harvesting in saturating light. By comparing how photosynthesis works in diverse organisms, we hope to uncover general design principles of natural photosynthesis as well as unique adaptations to different environments.

Algal biology

Eukaryotic algae and cyanobacteria (often collectively referred to simply as “algae”) are relatively simple phototrophic organisms that carry out oxygenic photosynthesis similar to that in land plants. Algae are amazingly diverse in terms of habitat, biochemistry, physiology, and morphology, and they have critical roles in global ecology and biogeochemistry. Aquatic microalgae (phytoplankton) are responsible for approximately half of the net primary production of organic matter on Earth, and they have recently re-emerged as potential next-generation feedstocks for biofuels (http://www.pbs.org/wgbh/nova/tech/algae-fuel.html).

Genetics and molecular biology

My lab uses genetic approaches to gain insight into the regulation of photosynthesis and photoprotection. We practice what I teach in Bio 1A -- everything from classical Mendelian genetics to the most cutting-edge genome editing tools. 

Courses

Bio 1A – General Biology
PMB 120 – Biology of Algae
PMB 120L – Biology of Algae Laboratory
PMB 290 – Plant and Microbial Photosynthesis

Publications

Recent work

García-Cerdán JG, Schmid EM, Takeuchi T, McRae I, McDonald K, Yordduangjun N, Hassan AM, Grob P, Xu CS, Hess HF, Fletcher DA, Nogales E, Niyogi KK (2020). Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and promotes carotenoid accumulation in Chlamydomonas. Proc Natl Acad Sci USA 117: 12452–12463. doi: 10.1073/pnas.1916948117

Hertle AP, García-Cerdán JG, Armbruster U, Shih R, Lee JJ, Wong W, Niyogi KK (2020). A Sec14 domain protein is required for photoautotrophic growth and chloroplast vesicle formation in Arabidopsis thaliana. Proc Natl Acad Sci USA 117: 9101-9111. doi: 10.1073/pnas.1916946117 (featured on the cover and in an accompanying Commentary)

Onoa B, Fukuda S, Iwai M, Bustamante C, Niyogi KK (2020). High-speed atomic force microscopy visualizes mobility of photosynthetic proteins in grana thylakoid membranes. Biophys J 118: 1876-1886. doi: 10.1016/j.bpj.2020.02.029

Arsenault EA, Yoneda Y, Iwai M, Niyogi KK, Fleming GR (2020). Vibronic mixing enables ultrafast energy flow in light-harvesting complex II. Nat Commun 11: 1460. doi: 10.1038/s41467-020-14970-1.

Dautermann O, Lyska D, Andersen-Ranberg J, Becker M, Gartmann H, Krämer LC, Mayr K, Pieper D, Rij LM, Niyogi KK, Lohr M (2020). An algal enzyme required for biosynthesis of the most abundant marine carotenoids. Sci Adv 6: eaaw9183. doi: 10.1126/sciadv.aaw9183

Amstutz CL, Fristedt R, Schultink A, Merchant SS, Niyogi KK, Malnoë A (2020). ROQH1 is a negative regulator of lipocalin-dependent non-photochemical quenching in Arabidopsis thaliana. Nature Plants 6: 154-166. doi: 10.1038/s41477-020-0591-9 

Roth MS, Westcott DJ, Iwai M, Niyogi KK (2019). Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga. Commun Biol 2: 347. doi: 10.1038/s42003-019-0577-1

Gabilly ST, Baker CR, Wakao S, Crisanto T, Guan K, Bi K, Guiet E, Guadagno CR, Niyogi KK (2019). Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS. Proc Natl Acad Sci USA 116: 17556-17562. doi: 10.1073/pnas.1821689116

García-Cerdán JG, Furst AL, McDonald KL, Schünemann D, Francis MB, Niyogi KK (2019). A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II. Proc Natl Acad Sci USA 116: 16631-16640. doi: 10.1073/pnas.1903314116

Roth MS, Gallaher SD, Westcott DJ, Iwai M, Louie KB, Mueller M, Walter A, Faflonker F, Bowen BP, Ataii NN, Song J, Chen J-H, Blaby-Haas CE, Larabell C, Auer M, Northen TR, Merchant SS, Niyogi KK. (2019). Regulation of oxygenic photosynthesis during trophic transitions in the green alga Chromochloris zofingiensis. Plant Cell 31: 579-601. doi: 10.1105/tpc.18.00742

Park S, Steen CJ, Lyska D, Fischer AL, Endelman B, Iwai M, Niyogi KK, Fleming GR (2019). Chlorophyll-carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis. Proc Natl Acad Sci USA 116: 3385-3390. doi: 10.1073/pnas.1819011116

Iwai M, Grob P, Iavarone AT, Nogales E, Niyogi KK (2018). A unique supramolecular organization of photosystem I in the moss Physcomitrella patens. Nature Plants 4: 904-909. doi: 10.1038/s41477-018-0271-1

Park S, Fischer AL, Steen C, Iwai M, Morris JM, Walla PJ, Niyogi KK, Fleming GR (2018). Chlorophyll-carotenoid excitation energy transfer in high-light-acclimating thylakoid membranes investigated by snapshot transient absorption spectroscopy. J Am Chem Soc 140: 11965-11973. doi: 10.1021/jacs.8b04844

Iwai M, Roth MS, Niyogi KK (2018). Subdiffraction-resolution live-cell imaging for visualizing thylakoid membranes. Plant J 96: 233-243. doi: 10.1111/tpj.14021

Leonelli L, Brooks MD, Niyogi KK (2017). Engineering the lutein epoxide cycle into Arabidopsis thaliana. Proc Natl Acad Sci USA 114: E7002-E7008. doi:10.1073/pnas.1704373114

Niyogi KK (2017). Physiology and metabolism: Light responses from photoreceptors to photosynthesis and photoprotection. Curr Opin Plant Biol 37: iv-vi. doi: 10.1016/j.pbi.2017.05.009

Xu CS, Hayworth KJ, Lu Z, Grob P, Hassan AM, García-Cerdan JG, Niyogi KK, Nogales E, Weinberg RJ, Hess HF (2017). Enhanced FIB-SEM systems for large-volume 3D imaging. eLife 6: e25916. doi: 10.7554/eLife.25916

Roth MS, Cokus SJ, Gallaher SD, Walter A, Lopez D, Erickson E, Endelman B, Westcott D, Larabell C, Merchant SS, Pellegrini M, Niyogi KK (2017). Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production. Proc Natl Acad Sci USA 114: E4296-E4305. doi: 10.1073/pnas.1619928114

Gee CW, Niyogi KK (2017). The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism in Nannochloropsis oceanica. Proc Natl Acad Sci USA 114: 4537-4542.

Kirst H, Gabilly ST, Niyogi KK, Lemaux PG, Melis A (2017). Photosynthetic antenna engineering to improve crop yields. Planta 245: 1009-1020.

Dall’Osto L, Cazzaniga S, Bressan M, Palecek D, Zidek K, Niyogi KK, Fleming GR, Zigmantas D, Bassi R (2017). Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nature Plants 3: 17033. doi: 10.1038/nplants.2017.33

Allorent G, Lefebvre-Legendre L, Chappuis R, Kuntz M, Truong TB, Niyogi KK, Ulm R, Goldschmidt-Clermont (2016). UV-B photoreceptor-mediated photoprotection of the photosynthetic machinery. Proc Natl Acad Sci USA 113: 14864-14869.

Kromdijk J, Glowacka K, Leonelli L, Gabilly S, Iwai M, Niyogi KK, Long SP (2016). Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354: 857-861.

Leonelli L, Erickson E, Lyska D, Niyogi KK (2016). Transient expression in Nicotiana benthamiana for rapid functional analysis of genes involved in non-photochemical quenching and carotenoid biosynthesis. Plant J 88: 375-386.

Li Z, Peers G, Dent RM, Bai Y, Yang SY, Apel W, Leonelli L, Niyogi KK (2016). Evolution of an atypical de-epoxidase for photoprotection in the green lineage. Nature Plants 2:16140. doi: 10.1038/nplants.2016.140.

Correa-Galvis V, Redekop P, Guan K, Grieß A, Truong TB, Wakao S, Niyogi KK, Jahns P (2016). PsbS is involved in the induction of LHCSR-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem 291: 17478-17487.

Armbruster U, Leonelli L, Correa-Galvis V, Strand D, Quinn E, Jonikas MC, Niyogi KK (2016). Regulation and levels of the thylakoid K+/H+ antiporter KEA3 shape the dynamic response of photosynthesis in fluctuating light. Plant Cell Physiol 57: 1557-1567.

Brzezowski P, Sharifi MN, Dent RM, Morhard MK, Niyogi KK, Grimm B (2016). Mg chelatase in chlorophyll synthesis and retrograde signaling in Chlamydomonas reinhardtii: CHLI2 cannot substitute for CHLI1. J Exp Bot 67: 3925-3938.

Ballottari M, Truong TB, De Re E, Erickson E, Stella GR, Fleming GR, Bassi R, Niyogi KK (2016). Identification of pH-sensing sites in the light harvesting complex stress-related 3 protein essential for triggering non-photochemical quenching in Chlamydomonas reinhardtii. J Biol Chem 291: 7334-7346.

Glowacka K, Kromkijk J, Leonelli L, Niyogi KK, Clemente TE, Long SP (2016). An evaluation of new and established methods to determine T-DNA copy number and homozygosity in transgenic plants. Plant Cell Environ 39: 908-917.

Tibiletti T, Hernández-Prieto MA, Matthijs HCP, Niyogi KK, Funk C (2016). Deletion of the gene family of small chlorophyll-binding proteins (ScpABCDE) offsets C/N homeostasis in Synechocystis PCC 6803. Biochim Biophys Acta 1857: 396-407.

Ngan CY, Wong C-H, Choi C, Yoshinaga Y, Louie K, Jia J, Chen C, Bowen B, Cheng H, Leonelli L, Kuo R, Baran R, García-Cerdán JG, Pratap, A, Wang, M, Lim J, Tice H, Daum C, Xu J, Northen T, Visel A, Bristow J, Niyogi KK, Wei C-L (2015). Lineage-specific chromatin signatures reveal a regulator of lipid metabolism in microalgae. Nature Plants 1: 15107. 

Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Lindstrom DL, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Spalding MH, van Wijk KJ, Vermaas WFJ, von Caemmerer S, Weber APM, Yeates TO, Yuan JS, Zhu XG (2015). Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA 112: 8529-8536.

Niyogi KK, Wolosiuk RA, Malkin R, (2015).  Photosynthesis. In: Biochemistry and Molecular Biology of Plants, 2nd edition, Buchanan BB, Gruissem W, Jones RL, eds (Chichester, UK: John Wiley & Sons, Ltd.), pp. 508-566.

Tietz S, Puthiyaveetil S, Enlow HM, Yarbrough R, Wood M, Semchonok D, Lowry T, Li Z, Jahns P, Boekema EJ, Lenhert S, Niyogi KK, Kirchhoff H (2015). Functional implications of photosystem II crystal formation in photosynthetic membranes. J Biol Chem 290: 14091-14106.

Erickson E, Wakao S, Niyogi KK (2015). Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J 82: 449-465.

Dent RM, Sharifi MN, Haglund C, Malnoë, A, Calderon RH, Wakao S, Niyogi KK (2015). Large-scale insertional mutagenesis of Chlamydomonas supports phylogenomic functional prediction of photosynthetic genes and analysis of classical acetate-requiring mutants. Plant J 82: 337-351.

Highlights of older work

Wakao S, Chin BL, Ledford HK, Dent RM, Casero D, Merchant SS, Pellegrini M, Niyogi KK (2014). Phosphoprotein SAK1 is a regulator of acclimation to singlet oxygen in Chlamydomonas reinhardtii. eLife 3: e02286. doi: 10.7554/eLife.02286

Shih PM, Zarzycki J, Niyogi KK, Kerfeld CA (2014).Introduction of a synthetic CO2-fixing photorespiratory bypass into a cyanobacterium. J Biol Chem 289: 9493-9500.

Calderon RH, García-Cerdán J, Malnoë A, Cook R, Russell JJ, Gaw C, Dent RM, de Vitry C, Niyogi KK (2013). A conserved rubredoxin is necessary for photosystem II accumulation in diverse oxygenic photoautotrophs. J Biol Chem 288: 26688-26696

Brooks MD, Sylak-Glassman EJ, Fleming GR, Niyogi KK (2013). A thioredoxin-like/beta-propeller protein maintains the efficiency of light harvesting in Arabidopsis. Proc Natl Acad Sci USA 110: E2733-2740. doi: 10.1073/pnas.1305443110

Niyogi KK, Truong TB (2013). Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Op Plant Biol 16: 307-314.

Zaks J, Amarnath K, Kramer DM, Niyogi KK, Fleming GR (2012). A kinetic model of rapidly reversible nonphotochemical quenching. Proc Natl Acad Sci USA 109: 15757-15762.

Amarnath K, Zaks J, Park SD, Niyogi KK, Fleming GR (2012). Fluorescence lifetime snapshots reveal two rapidly reversible mechanisms of photoprotection in live cells of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 109: 8405-8410. doi: 10.1073/pnas.1205303109

Fischer BB, Ledford HK, Wakao S, Huang SG, Casero D, Pellegrini M, Merchant SS, Koller A, Eggen RIL, Niyogi KK (2012). SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 109: E1302-1311. doi:10.1073/pnas.1116843109

Li Z, Keasling JD, Niyogi KK (2012). Overlapping photoprotective function of vitamin E and carotenoids in Chlamydomonas. Plant Physiol 158: 313-323. doi:10.1104/pp.111.181230 (featured in accompanying “On the Inside” article)

Kilian O, Benemann CSE, Niyogi KK, Vick B (2011). High-efficiency homologous recombination in the oil-producing alga, Nannochloropsis sp. Proc Natl Acad Sci USA 108: 21265-21269. doi:10.1073/pnas.1105861108 (featured on the cover and in an accompanying Commentary)

Murchie EH, Niyogi KK (2011). Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155: 86-92.

Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011). Analysis of LHCSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9(1): e1000577. doi:10.1371/journal.pbio.1000577

Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009). An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462: 518-52.

Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009). Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21: 1798-1812.

Li Z, Wakao S, Fischer BB, Niyogi KK (2009). Sensing and responding to excess light. Annu Rev Plant Biol 60: 239-260.

Ahn TK, Avenson TJ, Ballottari M, Cheng, Y-C, Niyogi KK, Bassi R, Fleming GR (2008). Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797.

Ledford HK, Chin BL, Niyogi KK (2007). Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot Cell 6: 919–930.

Dent RM, Haglund CM, Chin BL, Kobayashi MC, Niyogi KK (2005). Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol 137: 545–556.

Holt NE, Zigmantas D, Valkunas L, Li X-P, Niyogi KK, Fleming GR (2005). Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307: 433–436.

Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004). Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279: 22866–22874.

Müller-Moulé P, Golan T, and Niyogi KK (2004). Ascorbate-deficient mutants of Arabidopsis thaliana grow in high light despite chronic photo-oxidative stress. Plant Physiol 134: 1163–1172.

Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, Niyogi KK (2004). Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. J Biol Chem 279: 6337–6344.

Müller-Moulé P, Havaux M, Niyogi KK (2003). Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis thaliana. Plant Physiol 133: 748–760.

Ma Y-Z, Holt NE, Li X-P, Niyogi KK, Fleming GR (2003). Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100: 4377–4382.

Baroli I, Do AD, Yamane T, Niyogi KK (2003). Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photo-oxidative stress. Plant Cell 15: 992–1008.

Li X-P, Müller-Moulé P, Gilmore AM, Niyogi KK (2002). PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99: 15222–15227.

Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391–395.

Havaux M, Niyogi KK (1999).  The violaxanthin cycle protects plants from photo-oxidative damage by more than one mechanism.  Proc Natl Acad Sci USA 96:  8762–8767.

Honors and Awards

Elected Fellow of the American Association for the Advancement of Science (AAAS) - 2016
Elected Member of National Academy of Sciences - 2016
Fellow of ASPB Award - American Society of Plant Biologists - 2016
HHMI-GBMF Investigator - Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation - 2011
Charles Albert Schull Award - American Society of Plant Biologists - 2005
Melvin Calvin Award - International Society of Photosynthesis Research - 2001
Presidential Early Career Award for Scientists and Engineers - USDA - 1998
Searle Scholar - Searle Scholars Program/The Chicago Community Trust - 1998