Mari Ogawa-Ohnishi, Tomohide Yamashita, Mitsuru Kakita, Takuya Nakayama, Yuri Ohkubo, Yoko Hayashi, Yasuko Yamashita, Taizo Nomura, Saki Noda, Hidefumi Shinohara and Yoshikatsu Matsubayashi : Peptide ligand-mediated trade-off between plant growth and stress response., Science, Vol.378, No.6616, 175-180, 2022.
(要約)
Deciding whether to grow or to divert energy to stress responses is a major physiological trade-off for plants surviving in fluctuating environments. We show that three leucine-rich repeat receptor kinases (LRR-RKs) act as direct ligand-perceiving receptors for PLANT PEPTIDE CONTAINING SULFATED TYROSINE (PSY)-family peptides and mediate switching between two opposing pathways. By contrast to known LRR-RKs, which activate signaling upon ligand binding, PSY receptors (PSYRs) activate the expression of various genes encoding stress response transcription factors upon depletion of the ligands. Loss of PSYRs results in defects in plant tolerance to both biotic and abiotic stresses. This ligand-deprivation-dependent activation system potentially enables plants to exert tuned regulation of stress responses in the tissues proximal to metabolically dysfunctional damaged sites where ligand production is impaired.
Sota Fujii, Hiroko Shimosato-Asano, Mitsuru Kakita, Takashi Kitanishi, Megumi Iwano and Seiji Takayama : Parallel evolution of dominant pistil-side self-incompatibility suppressors in Arabidopsis, Nature Communications, Vol.11, No.1, 1404, 2020.
(要約)
Selfing is a frequent evolutionary trend in angiosperms, and is a suitable model for studying the recurrent patterns underlying adaptive evolution. Many plants avoid self-fertilization by physiological processes referred to as self-incompatibility (SI). In the Brassicaceae, direct and specific interactions between the male ligand SP11/SCR and the female receptor kinase SRK are required for the SI response. Although Arabidopsis thaliana acquired autogamy through loss of these genes, molecular evolution contributed to the spread of self-compatibility alleles requires further investigation. We show here that in this species, dominant SRK silencing genes have evolved at least twice. Different inverted repeat sequences were found in the relic SRK region of the Col-0 and C24 strains. Both types of inverted repeats suppress the functional SRK sequence in a dominant fashion with different target specificities. It is possible that these dominant suppressors of SI contributed to the rapid fixation of self-compatibility in A. thaliana.
John L. Bowman, Takayuki Kohchi, Katsuyuki T. Yamato, Jerry Jenkins, Shengqiang Shu, Kimitsune Ishizaki, Shohei Yamaoka, Ryuichi Nishihama, Yasukazu Nakamura, Frédéric Berger, Catherine Adam, Shiori Sugamata Aki, Felix Althoff, Takashi Araki, Mario A. Arteaga-Vazquez, Sureshkumar Balasubrmanian, Kerrie Barry, Diane Bauer, Christian R. Boehm, Liam Briginshaw, Juan Caballero-Perez, Bruno Catarino, Feng Chen, Shota Chiyoda, Mansi Chovatia, Kevin M. Davies, Mihails Delmans, Taku Demura, Tom Dierschke, Liam Dolan, Ana E. Dorantes-Acosta, Magnus D. Eklund, Stevie N. Florent, Eduardo Flores-Sandoval, Asao Fujiyama, Hideya Fukuzawa, Bence Galik, Daniel Grimanelli, Jane Grimwood, Ueli Grossniklaus, Takahiro Hamada, Jim Haseloff, Alexander J. Hetherington, Asuka Higo, Yuki Hirakawa, Hope N. Hundley, Yoko Ikeda, Keisuke Inoue, Shin-ichiro Inoue, Sakiko Ishida, Qidong Jia, Mitsuru Kakita, Takehiko Kanazawa, Yosuke Kawai, Tomokazu Kawashima, Megan Kennedy, Keita Kinose, Toshinori Kinoshita, Yuji Kohara, Eri Koide, Kenji Komatsu, Sarah Kopischke, Minoru Kubo, Junko Kyozuka, Ulf Lagercrantz, Shih-Shun Lin, Erika Lindquist, Anna M. Lipzen, Chia-Wei Lu, Efraín De Luna, Robert A. Martienssen, Naoki Minamino, Masaharu Mizutani, Miya Mizutani, Nobuyoshi Mochizuki, Isabel Monte, Rebecca Mosher, Hideki Nagasaki, Hirofumi Nakagami, Satoshi Naramoto, Kazuhiko Nishitani, Misato Ohtani, Takashi Okamoto, Masaki Okumura, Jeremy Phillips, Bernardo Pollak, Anke Reinders, Moritz Rövekamp, Ryosuke Sano, Shinichiro Sawa, Marc W. Schmid, Makoto Shirakawa, Roberto Solano, Alexander Spunde, Noriyuki Suetsugu, Sumio Sugano, Akifumi Sugiyama, Rui Sun, Yutaka Suzuki, Mizuki Takenaka, Daisuke Takezawa, Hirokazu Tomogane, Masayuki Tsuzuki, Takashi Ueda, Masaaki Umeda, John M. Ward, Yuichiro Watanabe, Kazufumi Yazaki, Ryusuke Yokoyama, Yoshihiro Yoshitake, Izumi Yotsui, Sabine Zachgo and Jeremy Schmutz : Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome., Cell, Vol.171, No.2, 287-304, 2017.
(要約)
The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PAPERCLIP.
Self-incompatibility in the Brassicaceae is controlled by multiple haplotypes encoding the pollen ligand (S-locus protein 11, SP11, also known as S-locus cysteine-rich protein, SCR) and its stigmatic receptor (S-receptor kinase, SRK). A haplotype-specific interaction between SP11/SCR and SRK triggers the self-incompatibility response that leads to self-pollen rejection, but the signalling pathway remains largely unknown. Here we show that Ca(2+) influx into stigma papilla cells mediates self-incompatibility signalling. Using self-incompatible Arabidopsis thaliana expressing SP11/SCR and SRK, we found that self-pollination specifically induced an increase in cytoplasmic Ca(2+) ([Ca(2+)]cyt) in papilla cells. Direct application of SP11/SCR to the papilla cell protoplasts induced Ca(2+) increase, which was inhibited by D-(-)-2-amino-5-phosphonopentanoic acid (AP-5), a glutamate receptor channel blocker. An artificial increase in [Ca(2+)]cyt in papilla cells arrested wild-type (WT) pollen hydration. Treatment of papilla cells with AP-5 interfered with self-incompatibility, and Ca(2+) increase on the self-incompatibility response was reduced in the glutamate receptor-like channel (GLR) gene mutants. These results suggest that Ca(2+) influx mediated by GLR is the essential self-incompatibility response leading to self-pollen rejection.
Xintian Lao, Keita Suwabe, Satoshi Niikura, Mitsuru Kakita, Megumi Iwano and Seiji Takayama : Physiological and genetic analysis of CO2-induced breakdown of self-incompatibility in Brassica rapa., Journal of Experimental Botany, Vol.65, No.4, 939-951, 2014.
(要約)
Self-incompatibility (SI) of the Brassicaceae family can be overcome by CO2 gas treatment. This method has been used for decades as an effective means to obtain a large amount of inbred seeds which can then be used for F1 hybrid seed production; however, the molecular mechanism by which CO2 alters the SI pathway has not been elucidated. In this study, to obtain new insights into the mechanism of CO2-induced SI breakdown, the focus was on two inbred lines of Brassica rapa (syn. campestris) with different CO2 sensitivity. Physiological examination using X-ray microanalysis suggested that SI breakdown in the CO2-sensitive line was accompanied by a significant accumulation of calcium at the pollen-stigma interface. Pre-treatment of pollen or pistil with CO2 gas before pollination showed no effect on the SI reaction, suggesting that some physiological process after pollination is necessary for SI to be overcome. Genetic analyses using F1 progeny of a CO2-sensitive × CO2-insensitive cross suggested that CO2 sensitivity is a semi-dominant trait in these lines. Analysis of F2 progeny suggested that CO2 sensitivity could be a quantitative trait, which is controlled by more than one gene. Quantitative trait locus (QTL) analyses identified two major loci, BrSIO1 and BrSIO2, which work additively in overcoming SI during CO2 treatment. No QTL was detected at the loci previously shown to affect SI stability, suggesting that CO2 sensitivity is determined by novel genes. The QTL data presented here should be useful for determining the responsible genes, and for the marker-assisted selection of desirable parental lines with stable but CO2-sensitive SI in F1 hybrid breeding.
Megumi Iwano, Tetsuyuki Entani, Hiroshi Shiba, Mitsuru Kakita, Takeharu Nagai, Hideaki Mizuno, Atsushi Miyawaki, Tsubasa Shoji, Kenichi Kubo, Akira Isogai and Seiji Takayama : Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth., Plant Physiology, Vol.150, No.3, 1322-1334, 2009.
(要約)
Pollen tube growth is crucial for the delivery of sperm cells to the ovule during flowering plant reproduction. Previous in vitro imaging of Lilium longiflorum and Nicotiana tabacum has shown that growing pollen tubes exhibit a tip-focused Ca(2+) concentration ([Ca(2+)]) gradient and regular oscillations of the cytosolic [Ca(2+)] ([Ca(2+)](cyt)) in the tip region. Whether this [Ca(2+)] gradient and/or [Ca(2+)](cyt) oscillations are present as the tube grows through the stigma (in vivo condition), however, is still not clear. We monitored [Ca(2+)](cyt) dynamics in pollen tubes under various conditions using Arabidopsis (Arabidopsis thaliana) and N. tabacum expressing yellow cameleon 3.60, a fluorescent calcium indicator with a large dynamic range. The tip-focused [Ca(2+)](cyt) gradient was always observed in growing pollen tubes. Regular oscillations of the [Ca(2+)](cyt), however, were rarely identified in Arabidopsis or N. tabacum pollen tubes grown under the in vivo condition or in those placed in germination medium just after they had grown through a style (semi-in vivo condition). On the other hand, regular oscillations were observed in vitro in both growing and nongrowing pollen tubes, although the oscillation amplitude was 5-fold greater in the nongrowing pollen tubes compared with growing pollen tubes. These results suggested that a submicromolar [Ca(2+)](cyt) in the tip region is essential for pollen tube growth, whereas a regular [Ca(2+)] oscillation is not. Next, we monitored [Ca(2+)] dynamics in the endoplasmic reticulum ([Ca(2+)](ER)) in relation to Arabidopsis pollen tube growth using yellow cameleon 4.60, which has a lower affinity for Ca(2+) compared with yellow cameleon 3.60. The [Ca(2+)](ER) in pollen tubes grown under the semi-in vivo condition was between 100 and 500 microm. In addition, cyclopiazonic acid, an inhibitor of ER-type Ca(2+)-ATPases, inhibited growth and decreased the [Ca(2+)](ER). Our observations suggest that the ER serves as one of the Ca(2+) stores in the pollen tube and cyclopiazonic acid-sensitive Ca(2+)-ATPases in the ER are required for pollen tube growth.
Mitsuru Kakita, Kohji Murase, Megumi Iwano, Tomohito Matsumoto, Masao Watanabe, Hiroshi Shiba, Akira Isogai and Seiji Takayama : Two distinct forms of MLPK localize to the plasma membrane and interact directly with SRK to transduce self-incompatibility signaling in Brassica rapa., The Plant Cell, Vol.19, No.12, 3961-3973, 2007.
(要約)
Many flowering plants possess systems of self-incompatibility (SI) to prevent inbreeding. In Brassica, SI recognition is controlled by the multiallelic gene complex (S-haplotypes) at the S-locus, which encodes both the male determinant S-locus protein 11 (SP11/SCR) and the female determinant S-receptor kinase (SRK). Upon self-pollination, the S-haplotype-specific interaction between the pollen-borne SP11 and the cognate stigmatic SRK receptor induces SI signaling in the stigmatic papilla cell and results in rejection of the self-pollen. Our genetic analysis of a self-compatible mutant revealed the involvement of a cytoplasmic protein kinase, M-locus protein kinase (MLPK), in the SI signaling, but its exact physiological function remains unknown. In this study, we identified two different MLPK transcripts, MLPKf1 and MLPKf2, which are produced using alternative transcriptional initiation sites and encode two isoforms that differ only at the N termini. While MLPKf1 and MLPKf2 exhibited distinct expression profiles, both were expressed in papilla cells. MLPKf1 localizes to the plasma membrane through its N-terminal myristoylation motif, while MLPKf2 localizes to the plasma membrane through its N-terminal hydrophobic region. Although both MLPKf1 and MLPKf2 could independently complement the mlpk/mlpk mutation, their mutant forms that lack the plasma membrane localization motifs failed to complement the mutation. Furthermore, a bimolecular fluorescence complementation assay revealed direct interactions between SRK and the MLPK isoforms in planta. These results suggest that MLPK isoforms localize to the papilla cell membrane and interact directly with SRK to transduce SI signaling.
(キーワード)
Alternative Splicing / Amino Acid Sequence / Base Sequence / Brassica rapa / Cell Membrane / Gene Expression Regulation, Plant / Genetic Complementation Test / In Situ Hybridization / Molecular Sequence Data / Mutation / Plant Proteins / Plants, Genetically Modified / Protein Binding / Protein Isoforms / Protein Kinases / Reverse Transcriptase Polymerase Chain Reaction / Sequence Alignment / Signal Transduction
Mitsuru Kakita, Tsunenori Shimizu, Masami Emoto, Mariya Nagai, Miyo Takeguchi, Yuuki Hosono, Nahoko Kume, Toshikatsu Ozawa, Mayuko Ueda, Islam Md. Shaidul Bhuiyan and Yoshinori Matsuo : Divergence and heterogeneity of the histone gene repeating units in the Drosophila melanogaster species subgroup., Genes & Genetic Systems, Vol.78, No.5, 383-389, 2003.