The Plant Journal

Cover image for Vol. 86 Issue 6

Early View (Online Version of Record published before inclusion in an issue)

Edited By: Christoph Benning

Impact Factor: 5.468

ISI Journal Citation Reports © Ranking: 2015: 13/209 (Plant Sciences)

Online ISSN: 1365-313X


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  1. Original Articles

    1. Root-specific expression of opine genes and opine accumulation in some cultivars of the naturally occurring genetically modified organism Nicotiana tabacum

      Ke Chen, François Dorlhac de Borne, Emilie Julio, Julie Obszynski, Patrick Pale and Léon Otten

      Version of Record online: 26 JUL 2016 | DOI: 10.1111/tpj.13196

      Significance Statement

      Several naturally occurring GMO plants have been described, belonging to the genera Nicotiana, Linaria and Ipomoea, several carry opine synthesis genes. Sofar, however, detectable levels of opines have not been demonstrated in such natural GMOs. We find that the cT-DNA TB-mas2’ gene is expressed at very low levels in most Nicotiana tabacum cultivars. However, in some cultivars TB-mas2’ is highly expressed in root tips giving detectable levels of the Amadori opine deoxyfructosyl-glutamine.

    2. Identification of a small protein domain present in all plant lineages that confers high prephenate dehydratase activity

      Jorge El-Azaz, Fernando de la Torre, Concepción Ávila and Francisco M. Cánovas

      Version of Record online: 26 JUL 2016 | DOI: 10.1111/tpj.13195

      Significance Statement

      Phenylalanine is essential for protein synthesis and as a precursor for metabolites such as lignin and flavonoids. Phenylalanine is synthesized by the arogenate pathway or by an alternative pathway, well studied in microorganisms, the phenylpyruvate pathway. Here we use a conifer to characterize the phenylpyruvate pathway and demonstrate that a conserved 20 amino acid domain in prephenate dehydratase is required for enzyme activity.

    3. RNA-directed DNA methylation efficiency depends on trigger and target sequence identity

      Athanasios Dalakouras, Elena Dadami, Michèle Wassenegger, Gabi Krczal and Michael Wassenegger

      Version of Record online: 26 JUL 2016 | DOI: 10.1111/tpj.13193

      Significance Statement

      RNA-directed DNA methylation (RdDM) is an important mechanism shaping the epigenome in plants, but the RNA molecule that triggers RdDM is still elusive Here, using a viroid-based system, we provide more support for the hypothesis that >24-nt RNAs recognize the target DNA and find that the efficiency of RdDM is proportional to the RNA:DNA homology.

  2. Resource

    1. The genome of black raspberry (Rubus occidentalis)

      Robert VanBuren, Doug Bryant, Jill M. Bushakra, Kelly J. Vining, Patrick P. Edger, Erik R. Rowley, Henry D. Priest, Todd P. Michael, Eric Lyons, Sergei A. Filichkin, Michael Dossett, Chad E. Finn, Nahla V. Bassil and Todd C. Mockler

      Version of Record online: 20 JUL 2016 | DOI: 10.1111/tpj.13215

      Significance Statement

      Black raspberry is an under-utilized specialty crop with great potential for breeding improvement. Its relationship to red raspberry, blackberry, and to other Rosaceae crops in general, will allow these resources to be widely used by breeders and researchers studying this important crop family.

  3. Original Articles

    1. You have full text access to this OnlineOpen article
      Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas

      Judith A. Irwin, Eleni Soumpourou, Clare Lister, Jan-Dick Ligthart, Sue Kennedy and Caroline Dean

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13221

      Being able to harvest different broccoli (Brassica oleracea) varieties throughout the year is a function of allelic differences at the floral repressor BoFLC.C2. Here, we show that epigenetic silencing and reactivation of expression after cold exposure of BoFLC.C2 are critical factors in this variation. Domestication in horticultural brassicas has therefore exploited similar cis polymorphism at FLC to that underpinning natural variation in Arabidopsis thaliana.

    2. Two polyketide synthases are necessary for 4-hydroxy-5-methylcoumarin biosynthesis in Gerbera hybrida

      Milla Pietiäinen, Juha Kontturi, Tanja Paasela, Xianbao Deng, Miia Ainasoja, Paulina Nyberg, Hannu Hotti and Teemu H. Teeri

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13216

      Significance Statement

      Coumarins are thought to play roles in plant defense, but the enzymes required for biosynthesis of the polyketide-derived 4-hydroxy-5-methylcoumarin were not known. Here we identify and characterize the responsible polyketide synthases.

    3. Inhibition of the Arabidopsis bHLH transcription factor by monomerization through abscisic acid-induced phosphorylation

      Yohei Takahashi, Toshinori Kinoshita, Masaki Matsumoto and Ken-ichiro Shimazaki

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13217

      The basic helix–loop–helix transcriptional activator, ABA-responsive kinase substrate 1 (AKS1), enhances K+ channel expression in guard cells leading to stomatal opening. Abscisic acid (ABA) induces monomerization of the AKS1 by phosphorylation through protein kinase of SnRK2.6, and results in release of AKS1 from DNA providing a mechanism of ABA-dependent repression of gene expression through phosphorylation.

    4. Repression of callus initiation by the miRNA-directed interaction of auxin–cytokinin in Arabidopsis thaliana

      Zhenhua Liu, Juan Li, Long Wang, Qiang Li, Qing Lu, Yanchong Yu, Shuo Li, Ming-yi Bai, Yuxin Hu and Fengning Xiang

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13211

      Callus formation is a striking example of plant cellular reprogramming, but the underlying genetic cues are poorly understood. Here we show that miR160 acts as a key repressor of callus formation by targeting an auxin transcription factor, ARF10, thus resulting in expression of the cytokinin signaling gene ARR15. Modulation of ARF10 expression by miR160 represents a molecular link between auxin and cytokinin signaling in cellular reprogramming.

    5. Imprinted gene OsFIE1 modulates rice seed development by influencing nutrient metabolism and modifying genome H3K27me3

      Xiaolong Huang, Zhanhua Lu, Xin Wang, Yidan Ouyang, Wei Chen, Koulong Xie, Dongying Wang, Min Luo, Jie Luo and Jialing Yao

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13202

      Imprinted Polycomb group genes play a critical role in seed development in Arabidopsis, but the roles of imprinted genes in cereals remain obscure. Here, we characterize a rice endosperm-specific Polycomb group gene OsFIE1, which influences transcription factor expression and nutrient metabolism in rice.

    6. The role of arabinokinase in arabinose toxicity in plants

      Robert Behmüller, Eva Kavkova, Stefanie Düh, Christian G. Huber and Raimund Tenhaken

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13206

      Cell wall polymers are synthesized by glycosyl transferases that require activated nucleotide sugars as substrates, and these polymers are degraded to monosaccharides and recycled to nucleotide sugars. Here we biochemically characterized arabinokinase and assess metabolites in arabinokinase knockout mutants, including the conditionally lethal ara1-1 mutant. Our results challenge the previous view of arabinose toxicity; we instead propose that arabinose toxicity in the ara1-1 mutant is more likely due to misinterpretation of sugar status by other kinases, rather than due to arabinose accumulation.

  4. Resource

    1. You have full text access to this OnlineOpen article
      Gene coexpression network analysis of oil biosynthesis in an interspecific backcross of oil palm

      Chloé Guerin, Thierry Joët, Julien Serret, Philippe Lashermes, Virginie Vaissayre, Mawussé D. T. Agbessi, Thierry Beulé, Dany Severac, Philippe Amblard, James Tregear, Tristan Durand-Gasselin, Fabienne Morcillo and Stéphane Dussert

      Version of Record online: 19 JUL 2016 | DOI: 10.1111/tpj.13208

      Significance Statement

      Global demand for vegetable oils is increasing, but our understanding of how oil biosynthesis is regulated remains limited. Here we used an interspecific backcross population of oil palm, transcript coexpression and transcript–metabolite correlations to identify novel enzymes, transcription factors and cellular processes involved in oil biosynthesis. Our findings should facilitate the development of novel breeding and engineering strategies in oil palm and other oil crops.

  5. Technical Advance

    1. You have full text access to this OnlineOpen article
      Mapping-by-sequencing in complex polyploid genomes using genic sequence capture: a case study to map yellow rust resistance in hexaploid wheat

      Laura-Jayne Gardiner, Pauline Bansept-Basler, Lisa Olohan, Ryan Joynson, Rachel Brenchley, Neil Hall, Donal M. O'Sullivan and Anthony Hall

      Version of Record online: 18 JUL 2016 | DOI: 10.1111/tpj.13204

      It is challenging to apply mapping-by-sequencing pipelines to large polyploid genomes such as hexaploid wheat. Here we present a method for the rapid mapping of genes responsible for a phenotype, and demonstrate its utility by mapping a disease resistance gene. We show that our bespoke mapping-by-sequencing pipeline, available on iPlant, can be applied to poorly defined polyploid genomes.

  6. Resource

    1. Aminooxy-naphthylpropionic acid and its derivatives are inhibitors of auxin biosynthesis targeting l-tryptophan aminotransferase: structure–activity relationships

      Megumi Narukawa-Nara, Ayako Nakamura, Ko Kikuzato, Yusuke Kakei, Akiko Sato, Yuka Mitani, Yumiko Yamasaki-Kokudo, Takahiro Ishii, Ken-ichiro Hayashi, Tadao Asami, Takehiko Ogura, Shigeo Yoshida, Shozo Fujioka, Takashi Kamakura, Tsutomu Kawatsu, Masanori Tachikawa, Kazuo Soeno and Yukihisa Shimada

      Version of Record online: 18 JUL 2016 | DOI: 10.1111/tpj.13197

      It is difficult to evaluate the functions of auxin and the biosynthesis pathways of indole-3-acetic acid using genetic approaches; chemical genetics is an alternative method. Here we show that L-α-aminooxy-phenylpropionic acid (AOPP), an inhibitor of auxin biosynthesis, targets tryptophan aminotransferase. We synthesized novel compounds derived from AOPP to study the structure–activity relationships of inhibitors of tryptophan aminotransferase in vitro, and identified some that were more potent, and more specific, in inhibiting auxin levels. We designate these compounds ‘pyruvamines’.

    2. The walnut (Juglans regia) genome sequence reveals diversity in genes coding for the biosynthesis of non-structural polyphenols

      Pedro J. Martínez-García, Marc W. Crepeau, Daniela Puiu, Daniel Gonzalez-Ibeas, Jeanne Whalen, Kristian A. Stevens, Robin Paul, Timothy S. Butterfield, Monica T. Britton, Russell L. Reagan, Sandeep Chakraborty, Sriema L. Walawage, Hans A. Vasquez-Gross, Charis Cardeno, Randi A. Famula, Kevin Pratt, Sowmya Kuruganti, Mallikarjuna K. Aradhya, Charles A. Leslie, Abhaya M. Dandekar, Steven L. Salzberg, Jill L. Wegrzyn, Charles H. Langley and David B. Neale

      Version of Record online: 18 JUL 2016 | DOI: 10.1111/tpj.13207

      Significance Statement

      In walnut, nut and wood quality are highly influenced by polyphenolic diversity, but the biosynthetic pathways for polyphenols are poorly characterized. Here we describe a high-quality draft genome sequence of the Persian walnut, Juglans regia, which will accelerate breeding and facilitate the genetic dissection of complex traits.

  7. Original Articles

    1. Identification of line-specific strategies for improving carotenoid production in synthetic maize through data-driven mathematical modeling

      Jorge Comas, Rui Benfeitas, Ester Vilaprinyo, Albert Sorribas, Francesc Solsona, Gemma Farré, Judit Berman, Uxue Zorrilla, Teresa Capell, Gerhard Sandmann, Changfu Zhu, Paul Christou and Rui Alves

      Version of Record online: 18 JUL 2016 | DOI: 10.1111/tpj.13210

      Significance Statement

      For the rational design of improved plants it is important to understand how engineered pathways interact with and are driven by endogenous metabolism. Here we combine experimental measurements with computational modeling and analysis to help understand these issues for carotenoid biosynthetic pathways.

  8. Resource

    1. Solanum pennellii backcross inbred lines (BILs) link small genomic bins with tomato traits

      Itai Ofner, Justin Lashbrooke, Tzili Pleban, Asaph Aharoni and Dani Zamir

      Version of Record online: 18 JUL 2016 | DOI: 10.1111/tpj.13194

      Wild species that are related to crop plants offer a means to understand the genetic basis of past domestication events and provide allelic diversity that can be used for future breeding of superior varieties. Here, we describe a high-resolution resource for tomato, which can be used to rapidly link genomic regions to phenotypes.

  9. Original Articles

    1. Diverse pathways of phosphatidylcholine biosynthesis in algae as estimated by labeling studies and genomic sequence analysis

      Naoki Sato, Natsumi Mori, Takashi Hirashima and Takashi Moriyama

      Version of Record online: 8 JUL 2016 | DOI: 10.1111/tpj.13199

      Significance Statement

      Phosphatidylcholine (PC) is nearly ubiquitous in eukaryotic algae and plants, but Chlamydomonas reinhardtii does not synthesize PC. Here we used comparative genomic analysis and radiolabeling to demonstrate the diversity of PC biosynthetic pathways in other Chlamydomonas species and in red algae. Our results suggest parallel losses of enzymes in some lineages.

  10. Technical Advance

    1. Strategy and software for the statistical spatial analysis of 3D intracellular distributions

      Eric Biot, Elizabeth Crowell, Jasmine Burguet, Herman Höfte, Samantha Vernhettes and Philippe Andrey

      Version of Record online: 8 JUL 2016 | DOI: 10.1111/tpj.13189

      Significance Statement

      Deciphering spatial organization within cells is challenging, because of the large morphological variations between cells. Here we present an algorithmic pipeline for normalizing variations in cell morphology and for statistically analyzing the spatial distributions of intracellular compartments from collections of 3D images, using endomembrane compartments in epidermal root cell cells as an example. Our analyses uncovered unsuspected polar distribution patterns not detectable in individual images. The approach and software should be generally applicable for modeling spatial organizations at multiple scales.

  11. Original Articles

    1. Evolutionary trajectory of phytoalexin biosynthetic gene clusters in rice

      Koji Miyamoto, Masahiro Fujita, Matthew R. Shenton, Shota Akashi, Chizu Sugawara, Arisa Sakai, Kiyotaka Horie, Morifumi Hasegawa, Hiroshi Kawaide, Wataru Mitsuhashi, Hideaki Nojiri, Hisakazu Yamane, Nori Kurata, Kazunori Okada and Tomonobu Toyomasu

      Version of Record online: 8 JUL 2016 | DOI: 10.1111/tpj.13200

      In plants, pathways for specialized metabolites are sometimes encoded by operon-like gene clusters. Here were use comparative genomics and biochemical studies in rice species to provide an evolutionary insight the mechanisms of formation of gene clusters encoding diterpene phytoalexins.

    2. Proteomics and metabolomics analyses reveal the cucurbit sieve tube system as a complex metabolic space

      Chaoyang Hu, Byung-Kook Ham, Hattem M. El-shabrawi, Danny Alexander, Dabing Zhang, John Ryals and William J. Lucas

      Version of Record online: 7 JUL 2016 | DOI: 10.1111/tpj.13209

      Significance Statement

      In angiosperms, it is well known that the phloem sieve tube system loads and delivers sugars, amino acids and signaling molecules to developing sinks and/or storage organs, but little is known about other metabolites that use this system. Here we show that the phloem sieve tube system also accumulates a broad range of metabolites, and that the enzymes and substrates for such metabolites are site specific.

    3. HSP90 canonical content organizes a molecular scaffold mechanism to progress flowering

      Theoni Margaritopoulou, Nikoleta Kryovrysanaki, Panagiota Megkoula, Constantinos Prassinos, Despoina Samakovli, Dimitra Milioni and Polydefkis Hatzopoulos

      Version of Record online: 7 JUL 2016 | DOI: 10.1111/tpj.13191

      A sophisticated gene network integrates environmental and endogenous cues in order to coordinate flowering. Here, we demonstrate that HEAT SHOCK PROTEIN 90 is essential for the vegetative-to-reproductive phase transition and flower development and counterbalances the extent to which developmental noise perturbs phenotypic traits.

    4. You have full text access to this OnlineOpen article
      Differential effector gene expression underpins epistasis in a plant fungal disease

      Huyen T.T. Phan, Kasia Rybak, Eiko Furuki, Susan Breen, Peter S. Solomon, Richard P. Oliver and Kar-Chun Tan

      Version of Record online: 7 JUL 2016 | DOI: 10.1111/tpj.13203

      Fungal necrotrophic effectors (NE) interact directly or indirectly with the products of dominant sensitivity/susceptibility genes in the plant. A successful interaction results in host tissue necrosis and/or chlorosis which promote pathogen infection. Epistasis of NEs is poorly understood. Here we use a fungal-wheat pathosystem to demonstrate that effector epistasis is due to interference with gene expression levels in the pathogen and not due to gene interactions in the host.

    5. Transfer RNA maturation in Chlamydomonas mitochondria, chloroplast and the nucleus by a single RNase P protein

      Géraldine Bonnard, Anthony Gobert, Mathilde Arrivé, Franziska Pinker, Thalia Salinas-Giegé and Philippe Giegé

      Version of Record online: 6 JUL 2016 | DOI: 10.1111/tpj.13198

      RNase P removes 5′ leader sequences of tRNA precursors. Here we demonstrate that Chlamydomonas has a single RNase P gene whose gene product acts in the chloroplast, mitochondria and the nucleus, thus contradicting the dogma that different RNase P systems act in each of these cellular compartments.

    6. Different flowering response to various fruit loads in apple cultivars correlates with degree of transcript reaccumulation of a TFL1-encoding gene

      Amnon Haberman, Michal Ackerman, Omer Crane, Jean-Jacques Kelner, Evelyne Costes and Alon Samach

      Version of Record online: 6 JUL 2016 | DOI: 10.1111/tpj.13190

      Significance Statement

      Biennial fruiting, also called alternate bearing, can affect fruit quality in heavy-bearing years and reduce yield in the subsequent sparce-bearing year. Here we use apple as a model to dissect the molecular events underlying alternate bearing; we show that the presence of adjacent fruit leads to reaccumulation of a flowering repressor in buds developing for the subsequent year. We further show that cultivars vary for this response, suggesting that cultivar-specific manipulations can improve annual fruit production.

    7. Analysis of gemini pollen 3 mutant suggests a broad function of AUGMIN in microtubule organization during sexual reproduction in Arabidopsis

      Sung-Aeong Oh, Jien Jeon, Hyo-Jin Park, Paul Eivind Grini, David Twell and Soon Ki Park

      Version of Record online: 6 JUL 2016 | DOI: 10.1111/tpj.13192

      Significance statement

      The AUGMIN complex is a conserved mediator of microtubule nucleation. Homozygous mutants in AUGMIN subunits have severe or lethal phenotypes. Here we characterized a mutant, gemini pollen 3 (gem3), with cell division defects during pollen mitosis I. We show that gem3 is a weak allele of AUGMIN6 and thus a valuable tool for investigating AUGMIN-dependent microtubule nucleation in plant cells.

  12. SI Synthetic Biology

    1. Towards engineering carboxysomes into C3 plants

      Maureen R. Hanson, Myat T. Lin, A. Elizabete Carmo-Silva and Martin A.J. Parry

      Version of Record online: 20 JUN 2016 | DOI: 10.1111/tpj.13139

      Significance Statement

      Photosynthesis in C3 plants is limited by features of the carbon-fixing enzyme Rubisco, which exhibits a low turnover rate and can also react with O2, leading to photorespiration. In cyanobacteria, bacterial microcompartments known as carboxysomes improve photosynthetic efficiency by concentrating CO2 near Rubisco. Thus transferring the carbon-concentrating mechanism from cyanobacteria to C3 plants is an attractive approach for improving crop photosynthesis. Here we review recent progress in engineering cyanobacterial β-carboxysomes into plant chloroplasts and in replacing C3 plant Rubisco with cyanobacterial Rubisco.

    2. Extending the biosynthetic repertoires of cyanobacteria and chloroplasts

      Agnieszka Zygadlo Nielsen, Silas Busck Mellor, Konstantinos Vavitsas, Artur Jacek Wlodarczyk, Thiyagarajan Gnanasekaran, Maria Perestrello Ramos H de Jesus, Brian Christopher King, Kamil Bakowski and Poul Erik Jensen

      Version of Record online: 20 JUN 2016 | DOI: 10.1111/tpj.13173

      Significance Statement

      Chloroplasts and cyanobacteria are increasingly popular chassis for metabolic engineering using synthetic biology. Photosynthetic reducing power, i.e. reduced ferredoxin, can be used to drive redox-dependent reactions and to redirect carbon precursors into new products, ranging from high-value pharmaceuticals to platform chemicals and fuels.

    3. Bacterial microcompartments as metabolic modules for plant synthetic biology

      C. Raul Gonzalez-Esquer, Sarah E. Newnham and Cheryl A. Kerfeld

      Version of Record online: 20 JUN 2016 | DOI: 10.1111/tpj.13166

      Significance Statement

      Bacterial microcompartments (BMCs) are metabolic modules that can be used in bioengineering to address pressing global issues such as food production, fossil fuel alternatives and climate change. In this review we describe progress towards reconfiguring BMCs through synthetic biology, for the development of novel nanoreactors in eukaryotic organisms (i.e. plants).

    4. You have full text access to this OnlineOpen article
      Synthetic redesign of plant lipid metabolism

      Richard P. Haslam, Olga Sayanova, Hae Jin Kim, Edgar B. Cahoon and Johnathan A. Napier

      Version of Record online: 20 JUN 2016 | DOI: 10.1111/tpj.13172

      Significance Statement

      In this review we advance the oilseed plant Camelina sativa as a useful platform for metabolic engineering of lipids, and propose that a new paradigm of predictive manipulation will exceed progress made thus far with iterative approaches.

    5. You have full text access to this OnlineOpen article
      Biotechnology and synthetic biology approaches for metabolic engineering of bioenergy crops

      Patrick M. Shih, Yan Liang and Dominique Loqué

      Version of Record online: 20 JUN 2016 | DOI: 10.1111/tpj.13176

    6. Engineering C4 photosynthesis into C3 chassis in the synthetic biology age

      Mara L. Schuler, Otho Mantegazza and Andreas P.M. Weber

      Version of Record online: 18 APR 2016 | DOI: 10.1111/tpj.13155

      Photosynthesis in C4 plants is more efficient than in C3 plants. Engineering aspects of C4 photosynthesis into C3 crop plants would enable major breakthroughs in increasing crop productivity. Here we review advances in understanding the molecular basis and evolution of the C4 trait, and discuss genetic tools and engineering approaches to achieve this goal.

    7. Synthetic biology for production of natural and new-to-nature terpenoids in photosynthetic organisms

      Philipp Arendt, Jacob Pollier, Nico Callewaert and Alain Goossens

      Version of Record online: 7 MAR 2016 | DOI: 10.1111/tpj.13138

      Terpenoids are the most complex group of specialized metabolites, and many are economically important pharmaceuticals, aromatics and potential next-generation biofuels. This review highlights the utility of photosynthetic organisms as platforms for the heterologous production of novel terpenoid structures, emphasizing how combinatorial biosynthesis and the activation of silent endogenous metabolism can be exploited to produce new-to-nature or tailor-made compounds.

  13. Synthetic Biology

    1. You have free access to this content
      Using CRISPR/Cas in three dimensions: towards synthetic plant genomes, transcriptomes and epigenomes

      Holger Puchta

      Version of Record online: 11 JAN 2016 | DOI: 10.1111/tpj.13100

      Genome editing with the bacterial RNA-based CRISPR (clustered regularly interspaced short palindromic repeats)/Cas9 system allows simultaneous targeting of multiple different enzyme activities to multiple independent sites in the genome and provides a framework for construction of at least partly synthetic entities at the genome, epigenome and transcriptome levels.


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