Reflections on Plant Cell Classics

In 2019, we are celebrating the 30th anniversary of The Plant Cell. In recognition of this milestone, we have solicted a series of reflections by members of the editorial board and others. We asked them to write about one or more memorable and exciting articles published in The Plant Cell, and how it influenced our current understanding.

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Editorial – Reflections on Plant Cell Classics by Sabeeha S. Merchant, Mary E. Williams and Nancy Eckardt

Editorial – The Plant Cell: Beginnings by Robert B. Goldberg, Brian A. Larkins, and Ralph S. Quatrano

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REFLECTIONS ON PLANT CELL CLASSICS

How Virus Resistance Provided a Mechanistic Foundation for RNA Silencing by David C. Baulcombe

• Lindbo, J.A., Silva-Rosales, L., Proebsting, W.M., and Dougherty, W.G. (1993). Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5: 1749–1759.

Genomic Balance Plays Out in Evolution by James A. Birchler

• Blanc, G. and Wolfe, K.H. (2004). Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16: 1679-1691.

Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation by Siobhan M. Brady

• Himanen, K., Boucheron, E., Vanneste, S., de Almeida Engler, J., Inze, D., and Beeckman, T. (2002). Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339-2351.

Auxin and organogenesis: Initiation of organs and nurturing a scientific spirit by Siobhan A. Braybrook

• Okada, K., Ueda, J., Komaki, M.K., Bell, C.J., and Shimura, Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677–684.
• Reinhardt, D., Mandel, T., and Kuhlemeier, C. (2000). Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12: 507–518.
• Reinhardt, D., Wittwer, F., Mandel, T., and Kuhlemeier, C. (1998). Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10: 1427–1437.

FLOWERING LOCUS C Isolation and Characterization: Two Papers that Opened Many Doors by George Coupland

• Michaels, S.D., and Amasino, R.M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
• Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J., and Dennis, E.S. (1999). The FLF MADS box gene: A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11: 445-458.

Genes Directing Flower Development in Arabidopsis by Elizabeth S. Dennis and William James Peacock

• Bowman, J.L., Smyth, D.R., and Meyerowitz, E. M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.

The Discovery of Plant D-type Cyclins by Lieven De Veylder

• Soni, R., Carmichael, J.P., Shah, Z.H., and Murray, J.A. (1995). A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85-103.

DREB Duo Defines Distinct Drought and Cold Response Pathways by Nancy Eckardt

• Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391-1406.
• Yamaguchi-Shinozaki, K, and Shinozaki, K. (1994). A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251-264.

RPN10: A Case Study for Ubiquitin-Binding Proteins and More by Pascal Genschik

• Smalle J, Kurepa J, Yang P, Emborg TJ, Babiychuk E, Kushnir S & Vierstra RD (2003) The pleiotropic role of the 26S Proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15: 965–980

Identification of cup-shaped cotyledon: New Ways to Think about Organ Initiation by Sarah Hake

• Aida M, Ishida T, Fukaki H, Fujisawa H, and Tasaka M. (1997). Genes involved in organ separation in arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841-857.

Auspicious Beginnings for the Defense Hormone Jasmonate by Gregg A. Howe

• Farmer, E.E. and Ryan, C.A. (1992). Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4: 129–134.
• Feys, B., Benedetti, C.E., Penfold, C.N., and Turner, J.G. (1994). Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751–759.

LOF and GOF alleles shed light on the molecular basis of phyB signaling in plants by Wei Hu and J. Clark Lagarias

• Reed J.W., Nagpal P., Poole D.S., Furuya M. & Chory J. (1993) Mutations in the gene for the red far-red light receptor phytochrome-B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell, 5: 147-157.
• Su Y.S. & Lagarias J.C. (2007) Light independent phytochrome signaling mediated by dominant GAF-domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell, 19: 2124-2139.

Flor-iculture: Ellis and Dodds’ Illumination of Gene-for-Gene Biology by Jonathan D. Jones

• Anderson, P.A., Lawrence, G.J., Morrish, B.C., Ayliffe, M.A., Finnegan, E.J., and Ellis JG. (1997). Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell. 9: 641-651. 
• Bernoux, M., Burdett, H., Williams, S.J., Zhang, X., Chen, C., Newell, K., Lawrence, G.J., Kobe, B., Ellis, J.G., Anderson, P.A., and Dodds, P.N. (2016). Comparative analysis of the flaximmune receptors L6 and L7 suggests an equilibrium-based switch activation model. Plant Cell 28: 146-159.
• Catanzariti, A.M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A., and Ellis, J.G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18: 243-256.
• Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Ayliffe, M.A., and Ellis, J.G. (2004). The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16: 755-768.
• Dodds, P.N., Lawrence, G.J., and Ellis, J.G. (2001). Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13: 163-178.
• Ellis, J.G., Lawrence, G.J., Luck, J.E., and Dodds, P.N. (1999). Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11: 495-506.
• Lawrence, G.J., Finnegan, E.J., Ayliffe, M.A., and Ellis, J.G. (1995). The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell. 7: 1195-206.
• Luck, J.E., Lawrence, G.J., Dodds, P.N., Shepherd, K.W., and Ellis JG. (2000).Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 12: 1367-1377.
• Wang, C.I., Guncar, G., Forwood, J.K., The, T., Catanzariti, A.M., Lawrence, G.J., Loughlin, F.E., Mackay, J.P., Schirra, H.J., Anderson, P.A., Ellis, J.G., Dodds, P.N., and Kobe, B. (2007). Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 19: 2898-2912.

Behind the Screen: How a Simple Seedling Response Helped Unravel Ethylene Signaling in Plants by Joseph J. Kieber and Eric Shaller

• Guzmán P & Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513-523.

Questionomics: Using Big Data to Ask and Answer Big Questions by Daniel J. Kliebenstein

• Reymond, P., Weber, H., Damond, M., and Farmer, E.E. (2000). Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707-719.
• Reymond, P., Bodenhausen, N., Van Poecke, R.M.P., Krishnamurthy, V., Dicke, M., and Farmer, E.E. (2004). A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16: 3132-3147.

Put on Your Sunscreen: The Birth of Arabidopsis Abiotic Stress Genetics by Robert L. Last

• Li, J., Ou-Lee, M., Amundson, R.G., and Last, R.L. (1993). Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5: 171 – 179.

Reflections on the issue of regulation in molecular and cellular biology by Cathie Martin and Richard A. Jorgensen

• Pichersky, E. (2006). Is the concept of regulation overused in molecular and cellular biology? Plant Cell 17: 3217-3218.

MicroRNAs in Plants: Key Findings from the Early Years by Blake C. Meyers, Michael J. Axtell

• Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
• Llave, C., Kasschau, K.D., Rector, M.A., and Carrington, J.C. (2002). Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605-1619.
• Sunkar, R., and Zhu, J.K. (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019.

Illuminating (White and) Purple Patches by Ortrun Mittelsten Scheid

• Napoli, C., Lemieux, C., and Jorgensen, R.A. (1990). Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2: 279-289.
• van der Krol, R.A., Mur, L.A., Mol, J.N.M., and Stuitje, A.R. (1990). Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2: 291-299.

Dissecting the Biological Functions of ARF and Aux/IAA Genes by Naomi Ori

• Okushima Y., Fukaki H., Onoda M., Theologis A., and Tasaka M. (2007). ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19: 118–130.
• Overvoorde P.J., Okushima Y., Alonso J.M., Chan A., Chang C., Ecker J.R., Hughes B., Liu A., Onodera C., Quach H., Smith A., Yu G. and  Theologis A. (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17: 3282–3300.

Early Leads to Mechanisms of Plant Cultivar-Specific Disease Resistance by Jane E. Parker

• Dong, X., Mindrinos, M., Davis, K.R., and Ausubel, F.M. (1991). ). Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3: 61-72.
• Whalen, M.C., Innes, R.W., Bent, A.F., and Staskawicz, B.J. (1991). Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49-59.

Reverse-Genetics of IRT1, or How to Catch an Iron Transporter and Pin It Down by Patrice A Salomé

• Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.-L., Briat, J.-F., and Curie, C. (2002). IRT1, an Arabidopsis Transporter Essential for Iron Uptake from the Soil and for Plant Growth. Plant Cell 14: 1223–1233.

Signal Transduction in Systemic Immunity by Steven H. Spoel

• Cao, H., Bowling, S.A., Gordon, A.S., and Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592.

From Ethylene-Auxin Interactions to Auxin Biosynthesis and Signal Integration by Anna N. Stepanova and Jose M. Alonso

• Ruzicka, K., Ljung, K., Vanneste, S., Podhorska, R., Beeckman, T., Friml, J., and Benkova, E. (2007). Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19: 2197-2212.
• Stepanova, A.N., Hoyt, J.M., Hamilton, A.A., and Alonso, J.M. (2005). A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17: 2230-2242.
• Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M.J. (2007). Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19: 2186-2196.

The Emergence of a Mobile Signal for Systemic Acquired Resistance by Hainan Tian and Yuelin Zhang

• Navarova H, Bernsdorff F, Doring AC, Zeier J. 2012. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24: 5123-5141.

Understanding the Molecular Bases of Agronomic Trait Improvement in Rice by Bing Wang and Jiayang Li

• Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., Koshioka, M., Futsuhara, Y., Matsuoka, M., and Yamaguchi, J. (2001). slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13: 999-1010.
• Li, Y., Qian, Q., Zhou, Y., Yan, M., Sun, L., Zhang, M., Fu, Z., Wang, Y., Han, B., Pang, X., Chen, M., and Li, J. (2003). BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15: 2020-2031.
• Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J., and Wang, Y. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512-1525.
• Wang, Z., Zou, Y., Li, X., Zhang, Q., Chen, L., Wu, H., Su, D., Chen, Y., Guo, J., Luo, D., Long, Y., Zhong, Y., and Liu, Y.G. (2006). Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18: 676-687.
• Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba, T., Yamamoto, K., Umehara, Y., Nagamura, Y., and Sasaki, T. (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12: 2473-2484.

All in the Family: The First Whole-genome Survey of NLR Genes by Detlef Weigel

• Meyers, B.C., Kozik, A., Griego, A., Kuang, H., and Michelmore, R.W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809–834.
• Pnueli, L., Gutfinger, T., Hareven, D., Ben-Naim, O., Ron, N., Adir, N., and Lifschitz, E. (2001). ). Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13: 2687–702.