College of Agriculture & Natural Resources Department of Horticulture

This program provides a 10-week research intensive experience in plant genomics to undergraduates entering their sophomore, junior or senior years. The  program is designed to enrich the professional development of participants and provide an insight to what life is like in graduate school.

Research

The Evolution of Biochemical Diversity within the Solanaceae

Plants are master chemists that collectively synthesize thousands of metabolites. These metabolites fall into two distinct classes; primary metabolites that are common to most plant lineages such as sugars, amino acids and fatty acids together with specialized metabolites (formerly, secondary metabolites) that are often lineage or species specific. Specialized metabolites are chemically diverse and include broad classes of structurally distinct molecules such as terpenoids, flavonoids and alkaloids. Many specialized metabolites are implicated in plant responses to abiotic or biotic stress and can serve directly as toxins or repellants. Alternatively, specialized metabolites, particularly those associated with the color and aroma of flowers and fruits serve as attractants to pollinators or seed dispersing fauna. As such, specialized metabolites are often synthesized in specific organs or cell types at particular stages of development or in response to environmental perturbation. Humans have exploited plant specialized metabolites for millennia for use as flavorings, fragrances, medicines, and poisons.

The Solanaceae (nightshade family) is a large and diverse family of approximately 3000 species that occupy varied ecological niches including species that thrive in tropical rain forests, at high altitudes in the mountain ranges of the Andes, and in desert environments. In addition, several Solanaceae species are important crop plants including potato, tomato, pepper, eggplant, tobacco and petunia. The Solanaceae family also exhibits tremendous phenotypic variation, including prolific diversity of specialized metabolites that often show restricted distribution to particular genera or species, or even to specific accessions within a species. This chemical diversity is fueled by rapid gene evolution that generates copy number variation leading to relaxed selection and subsequent neofunctionalization. We are utilizing an integrated approach involving genomics, metabolite profiling, gene-silencing biochemical analyses and synthetic biology to investigate the biosynthesis and evolution of specialized metabolite pathways within the Solanaceae. Current research is focused on the synthesis of defense compounds such as terpenes and acylsugars in the glandular trichomes and the biosynthesis of the medicinally important tropane alkaloids that occurs within the roots of selected members of the Solanaceae family. More information about our research can be found here: https://trichome.natsci.msu.edu/

Publications

Parks HM, Cinelli MA, Bedewitz MA, Grabar JM, Hurney SM, Walker KD, Jones AD, Barry CS (2023) Redirecting tropane alkaloid metabolism reveals pyrrolidine alkaloid diversity in Atropa belladonna. New Phytologist 237: 1810-1825 https://doi.org/10.1111/nph.18651

Sadre R, Anthony TM, Grabar JM, Bedewitz MA, Jones AD, Barry CS (2022) Metabolomics-guided discovery of cytochrome P450s involved in pseudotropine-dependent biosynthesis of modified tropane alkaloids. Nature Communications 13: 3832 https://doi.org/10.1038/s41467-022-31653-1

Fiesel PD, Parks HM, Last RL, Barry CS (2022) Fruity, Sticky, Stinky, Spicy, Bitter, Addictive and Deadly: Evolutionary Signatures of Metabolic Complexity in the Solanaceae. Natural Product Reports 39: 1438-1464 https://doi.org/10.1039/D2NP00003B

Wang P, Moore BM, Uygun S, Lehti-Shiu M, Barry CS, Shiu S-H (2021) Optimizing the use of gene expression data to predict plant metabolic pathway memberships. New Phytologist 231: 475-489 https://doi.org/10.1111/nph.17355

Moore BM, Wang P, Fan P, Lee A, Leong B, Lou Y-R, Schenck CA, Sugimoto K, Last RL, Lehti-Shiu M, Barry CS, Shiu S-H (2020) Within and cross-species predictions of plant specialized metabolism genes using transfer learning. In Silico Plants 2: diaa005 https://doi.org/10.1093/insilicoplants/diaa005

Rett-Cadman S, Colle M, Mansfeld B, Barry CS, Wang Y, Weng Y, Gao L, Fei Z, Grumet R (2019) QTL and transcriptomic analyses implicate cuticle transcription factor SHINE as a source of natural variation for epidermal traits in cucumber fruit. Frontiers in Plant Science 10: article number 1536 https://doi.org/10.3389/fpls.2019.01536

Wrenbeck EE, Bedewitz MA, Klesmith JR, Noshin S, Barry CS, Whitehead TA (2019) An automated data-driven pipeline for improving heterologous enzyme expression. ACS Synthetic Biology 8: 474-481. https://pubs.acs.org/doi/10.1021/acssynbio.8b00486

Bedewitz MA, Jones AD, D'Auria JC, Barry CS (2018) Tropinone synthesis via an atypical polyketide synthase and P450-mediated cyclization. Nature Communications 9: article number 5281. https://doi.org/10.1038/s41467-018-07671-3

Xu H, Moghe G, Wiegert-Rininger KE, Schilmiller AL, Barry CS, Last RL, Pichersky E (2018) Coexpression analysis identifies two oxidoreductases involved in the biosynthesis of the monoterpene acid moiety of natural pyrethrin insecticides in Tanacetum cinerariifolium. Plant Physiology: 176: 524-537. DOI: https://doi.org/10.1104/pp.17.01330  

Nadakuduti SS, Uebler JB, Liu X, Jones AD, Barry CS (2017) Characterization of trichome-expressed BAHDs in Petunia reveals distinct acylsugar assembly  mechanisms. Plant Physiology 175: 36-50. DOI: https://doi.org/10.1104/pp.17.00538 

Liu X, Enright M, Barry CS, Jones A (2017) Profiling, isolation and structure elucidation of specialized acylsucrose metabolites accumulating in trichomes of Petunia species. Metabolomics 13: article 85. doi:10.1007/s11306-017-1224-9

Bombarely A, Moser M, Amrad A, Bao M, Bapaume L, Barry CS et al., (2016) Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nature Plants Article Number 16074.

Guo Y,  Wiegert-Rininger KE, Vallejo VA, Barry CS, Warner RM (2015) Transcriptome-enabled marker discovery and mapping of plastochron-related genes in Petunia spp. BMC Genomics 16: 726

Vallejo VA, Tychonievich J, Lin W-K, Wangchu L, Barry CS, Warner RM (2015) Identification of QTL for crop timing and quality traits in an interspecific Petunia population. Molecular Breeding 35: 2 DOI 10.1007/s11032-015-0218-4.

Bedewitz MA, Góngora-Castillo E,  Uebler JB, Gonzales-Vigil E, Wiegert-Rininger KE, Childs KL, Hamilton JP, Vaillancourt B, Yeo YS, Chappell J, DellaPenna D, Jones AD, Buell CR, Barry CS (2014) A root-expressed L-phenylalanine:4-hydroxyphenylpyruvate aminotransferase is required for tropane alkaloid biosynthesis in Atropa belladonna. Plant Cell 26: 3745-3762.

Nadakuduti SS, Holdsworth WL, Klein CL, Barry CS (2014) KNOX genes influence a gradient of fruit chloroplast development through regulation of GOLDEN2-LIKE expression in tomato. Plant Journal 78: 1022-1033.

Kang J-H, Gonzales-Vigil E, Matsuba Y, Pichersky E, Barry CS (2014) Determination of residues responsible for substrate and product specificity of Solanum habrochaites short-chain cis-prenyltransferases. Plant Physiology 164: 80-91. 

Tychonievich J, Wangchu L, Barry C, Warner RM (2013) Utilizing wild species for marker-assisted selection of crop timing and quality traits in petunia. Acta Horticulturae 1000: 465-470.

Matsuba Y, Nguyen TTH, Wiegert K, Falara V, Gonzales-Vigil E, Leong B, Schäfer P, Kudrna D, Wing RA, Bolger AM, Usadel B, Tissier A, Fernie AR, Barry CS, Pichersky E (2013) Evolution of a complex locus for terpene biosynthesis in Solanum. Plant Cell 25: 2022-2036.

Kim J, Kang K, Gonzales-Vigil E, Shi F, Jones AD, Barry CS, Last RL (2012) Striking natural diversity in glandular trichome acylsugar composition is shaped by variation at the Acyltransferase 2 locus in the wild tomato Solanum habrochaites. Plant Physiology 160: 1854-1870.

Ma Q, Du W, Brandizzi F, Giovannoni JJ, Barry CS (2012) Differential control of ethylene responses by GREEN-RIPE and GREEN-RIPE LIKE1 provides evidence for distinct ethylene signaling modules in tomato. Plant Physiology 160: 1968-1984.

Powell ALT, Nguyen CV, Hill T, Cheng KLL, Figueroa‐Balderas R, Aktas H, Ashrafi H, Pons C, Fernández‐Muñoz R, Vicente A, Lopez‐Baltazar J, Barry CS, Liu Y, Chetelat R, Granell‐Richart A, Van Deynze A, Giovannoni JJ, Bennett AB (2012) Uniform ripening (U) encodes a Golden 2‐like transcription factor regulating tomato fruit chloroplast development. Science 336: 1711-1715.

Barry CS, Aldridge GM, Herzog G, Ma Q, McQuinn RP, Hirschberg J, Giovannoni JJ (2012) Altered chloroplast development and delayed fruit ripening caused by mutations in a chloroplast targeted zinc metalloprotease at the lutescent 2 locus of tomato. Plant Physiology 159: 1086-1098.

Nadakuduti SS, Pollard M, Kosma DK, Allen C Jr., Ohlrogge JB, Barry CS (2012) Pleiotropic phenotypes of the sticky peel (pe) mutant of tomato provide new insight into the role of CUTIN DEFICIENT 2. Plant Physiology 159: 945-960.

Gonzales-Vigil E, Hufnagel DE, Kim J, Last RL, Barry CS (2012) Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites. Plant Journal 71: 921-935.

Barry CS, Pandey P (2009) A survey of cultivated heirloom tomato varieties identifies four new mutant alleles at the green-flesh locus. Molecular Breeding 24: 269-276.

Barry CS (2009) The stay-green revolution: recent progress in deciphering the mechanisms of chlorophyll degradation in higher plants. Plant Science 176: 325 - 333.

Barry CS, McQuinn R, Chung M-Y, Besuden A, Giovannoni JJ (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiology 147: 179 - 187.

Barry CS, Giovannoni JJ. (2007) Ethylene and fruit ripening. Journal of Plant Growth Regulation. 26: 143 - 159.

Barry CS, Giovannoni JJ. (2006) Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci USA. 103: 7923-7928.

Barry CS, McQuinn R, Thompson AJ, Seymour GB, Grierson D, Giovannoni JJ (2005) Ethylene insensitivity conferred by the Green-ripe (Gr) and Never-ripe 2 (Nr-2) mutants of tomato. Plant Physiol 138: 267-275.

Adams-Phillips L, Barry C, Giovannoni J. (2004) Signal transduction systems regulating fruit ripening. Trends In Plant Science 9: 331-338.

Adams-Phillips L, Barry C, Kannan P, Leclercq J, Bouzayen M, Giovannoni J (2004) Evidence that CTR1-mediated ethylene signal transduction in tomato is encoded by a multigene family whose members display distinct regulatory features. Plant Mol Biol 54: 387-404.

Liu Y, Roof S, Ye Z, Barry C, Van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101: 9897-9902.

Moeder W, Barry CS, Tauriainen A, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjärvi J (2002) Ethylene synthesis regulated by bi-phasic induction of ACC synthase and ACC oxidase genes is required for H₂O₂ accumulation and cell death in ozone-exposed tomato. Plant Physiol 130: 1918-1926.

Barry CS, Fox EA, Yen H-C, Lee S, Ying T-J, Grierson D, Giovannoni JJ (2001) Analysis of the ethylene response in the epinastic (epi) mutant of tomato. Plant Physiol 127: 58-66.

Barry CS, Llop-Tous I, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123: 979-986.

Llop-Tous I, Barry CS, Grierson D (2000) Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiol. 123: 971-978.

Thompson AJ, Tor M, Barry CS, Vrebalov J, Orfila C, Jarvis MC, Giovannoni JJ, Grierson D, Seymour GB (1999) Molecular and genetic characterisation of a novel pleiotropic tomato-ripening mutant. Plant Physiol. 120: 383-389.

Griffiths A, Barry CS, Alpuche-Solis A, Grierson D (1999) Ethylene and developmental signals regulate expression of lipoxygenase genes during tomato fruit ripening. J. Ex. Bot. 50: 793-798.

Cooper W, Bouzayen M, Hamilton AJ, Barry CS, Rossall S, Grierson D (1998) Use of transgenic plants to study the role of ethylene and polygalacturonase during infection of tomato fruit by Colletotrichum gloeosporioides. Plant Pathology 47: 308-316.

Blume B, Barry CS, Hamilton AJ, Bouzayen M, Grierson D (1997) Identification of transposon-like elements in non-coding regions of tomato ACC oxidase genes. Mol. Gen. Genet. 254: 297-303.

Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D  (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant Journal 9: 525-535.

Postdoctoral Research Associates

Graduate Students

Levi Bauer, Genetics Program, 2018 - present

Hannah Parks, Biochemistry & Molecular Biology & Molecular Plant Sciences Programs, 2019 - present

Undergraduate Students

• Joe Reamsnyder, 2021 - present