Genomics of turions from the Greater Duckweed reveal its pathways for dormancy and re-emergence strategy.
cytosine methylation
dormancy
duckweed
germination
lipids
organelle copy number
triacylglycerol
turion
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
received:
22
11
2022
accepted:
24
03
2023
medline:
2
6
2023
pubmed:
7
5
2023
entrez:
7
5
2023
Statut:
ppublish
Résumé
Over 15 families of aquatic plants are known to use a strategy of developmental switching upon environmental stress to produce dormant propagules called turions. However, few molecular details for turion biology have been elucidated due to the difficulties in isolating high-quality nucleic acids from this tissue. We successfully developed a new protocol to isolate high-quality transcripts and carried out RNA-seq analysis of mature turions from the Greater Duckweed Spirodela polyrhiza. Comparison of turion transcriptomes to that of fronds, the actively growing leaf-like tissue, were carried out. Bioinformatic analysis of high confidence, differentially expressed transcripts between frond and mature turion tissues revealed major pathways related to stress tolerance, starch and lipid metabolism, and dormancy that are mobilized to reprogram frond meristems for turion differentiation. We identified the key genes that are likely to drive starch and lipid accumulation during turion formation, as well as those in pathways for starch and lipid utilization upon turion germination. Comparison of genome-wide cytosine methylation levels also revealed evidence for epigenetic changes in the formation of turion tissues. Similarities between turions and seeds provide evidence that key regulators for seed maturation and germination were retooled for their function in turion biology.
Substances chimiques
Starch
9005-25-8
Lipids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
116-131Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Adamec L. 2018. Ecophysiological characteristics of turions of aquatic plants: a review. Aquatic Botany 148: 64-77.
Ali F, Qanmber G, Li F, Wang Z. 2021. Updated role of ABA in seed maturation, dormancy, and germination. Journal of Advanced Research 35: 199-214.
Aoyagi BY, Kusumi J, Satake A. 2021. Copy number analyses of DNA repair genes reveal the role of poly (ADP-ribose) polymerase (PARP) in tree longevity. iScience 24: 102779.
Appenroth KJ. 2002. Co-action of temperature and phosphate in inducing turion formation in Spirodela polyrhiza (Great duckweed). Plant, Cell & Environment 25: 1079-1085.
Appenroth KJ, Gabrys H. 2001. Light-induced starch degradation in non-dormant turions of Spirodela polyrhiza. Photochemical Photobiology 73: 77-82.
Appenroth KJ, Hertel W, Jungnickel F, Augsten H. 1989a. Influence of nutrient deficiency and light on turion formation in Spirodela polyrhiza (L.) Schleiden. Biochemie und Physiologie der Pflanzen 184: 395-403.
Appenroth KJ, Keresztes A, Fischer W, Krzysztofowicz E, Gabrys H. 2011. Light-induced degradation of starch granules in turions of Spirodela polyrhiza studied by electron microscopy. Plant Cell Physiology 52: 384-391.
Appenroth KJ, Nickel G. 2010. Turion formation in Spirodela polyrhiza: the environmental signals that induce the developmental process in nature. Physiologia Plantarum 138: 312-320.
Appenroth KJ, Opfermann J, Hertel W, Augsten H. 1989b. Photophysiology of turion germination in Spirodela polyrhiza (L.) SCHLEIDEN. II. Influence of after-ripening on germination kinetics. Journal of Plant Physiology 135: 274-279.
Appenroth KJ, Ziegler P. 2008. Light-induced degradation of storage starch in turions of Spirodela polyrhiza depends on nitrate. Plant, Cell & Environment 10: 1460-1469.
Baggs EL, Tiersma MB, Abramson BW, Michael TP, Krasileva KV. 2022. Characterization of defense responses against bacterial pathogens in duckweeds lacking EDS1. New Phytologist 236: 1838-1855.
Bröker JN, Laibach N, Muller B, Prufer D, Gronover CS. 2018. Taraxacum brevicorniculatum rubber elongation factor TbREF associates with lipid droplets and affects lipid turn-over in yeast. Biotechnology Reports 20: e00290.
Carillo-Barral N, del Carmen R-GM, Matilla AJ. 2020. Delay of Germination-1 (DOG1): a key to understanding seed dormancy. Plants 9: 480.
Ding M, Wang L, Zhan W, Sun G, Jia X, Chen S, Ding W, Yang J. 2021. Genome-wide identification and expression analysis of late embryogenesis abundant protein-encoding genes in rye (Secale cereale L.). PLoS ONE 16: e0249757.
Dobritzsch M, Lubken T, Eschen-Lippold L, Gorzolka K, Blum E, Matern A, Marillonnet S, Bottcher C, Drager B, Rosahl S. 2016. MATE transporter-dependent export of hydroxycinnamic acid amides. Plant Cell 28: 583-596.
Gambino G, Perrone I, Gribaudo I. 2008. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochemical Analysis 19: 520-525.
González-Guzmán M, Apostolova N, Belles JM, Barrero JM, Pique P, Ponce MR, Micol JL, Serrano R, Rodriguez PL. 2002. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14: 1833-1846.
Graham IA. 2008. Seed storage oil mobilization. Annual Review Plant of Biology 59: 115-142.
Harkess A, McLaoughlin F, Biker N, Elliott K, Emenrcker R, Mattoon E, Miler K, Czymmek VRD, Meyers BC, Michael T. 2021. Improved Spirodela polyrhiza genome and proteomic analyses reveal a conserved chromosomal structure with high abundance of chloroplastic proteins favoring energy production. Journal of Experimental Botany 72: 2491-2500.
Hoang PNT, Michael TP, Gilbert S, Chu P, Motley ST, Appenroth KJ, Schubert I, Lam E. 2018. Generating a high-confidence reference genome map of the Greater Duckweed by integration of cytogenomic, optical mapping, and Oxford Nanopore technologies. The Plant Journal 96: 670-684.
Hong GJ, Yue XY, Mao YB, Wang LJ, Chen XY. 2012. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 224: 2635-2648.
Hundertmark M, Hincha DK. 2018. LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9: 118.
Jacobs DL. 1947. An ecological life-history of Spirodela polyrrhiza (greater duckweed) with emphasis on the turion phase. Ecological Monographs 17: 437-469.
Jansen HT, Trojahn S, Saxton MW, Quackenbush CR, Hutzeniler EBD, Nelson L, Cornejo OE, Robbins CT, Kelley JL. 2019. Hibernation induces widespread transcriptional remodeling in metabolic tissues of the grizzly bear. Communication Biology 2: 336.
Jühling F, Kretzmer H, Bernhart SH, Otto C, Stadler PF, Hoffmann S. 2016. Metilene: fast and sensitive calling of differentially methylated regions from bisulfite sequencing data. Genome Research 26: 256-262.
Kang IH, Steffen JG, Portereiko MF, Lyloyd A, Drews GN. 2008. The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20: 635-647.
Kawakatsu T, Nery JR, Castanon EJR. 2017. Dynamic DNA methylation reconfiguration during seed development and germination. Genome Biology 18: 171.
Kim JH, Nguyen NH, Jeong CY, Nguyen NT, Hong S-W, Lee H. 2013. Loss of the R2R3 MYB, AtMyb73, causes hyper-induction of the SOS1 and SOS3 genes in response to high salinity in Arabidopsis. Journal of Plant Physiology 170: 1461-1465.
Knoth C, Eulgem T. 2008. The oomycete response gene LURP1 is required for defense against Hyaloperonospora parasitica in Arabidopsis thaliana. The Plant Journal 55: 53-64.
Kuehdorf K, Jetschke G, Ballani L, Appenroth KJ. 2014. The clonal dependence of turion formation in the duckweed Spirodela polyrhiza - an ecogeographical approach. Physiology Plant 150: 46-54.
Landolt E. 1986. Biosystematic investigations in the family of duckweeds (Lemnaceae) (vol. 2). The family of Lemnaceae - a monographic study. Vol. 1. Zurich, Switzerland: Veroff Geobot. Inst. ETH.
Landolt E, Kandeler R. 1987. The family of Lemnaceae - a monographic study, 2. Biosystematic investigations in the family of duckweeds (Lemnaceae). Zurich, Switzerland: Veroff Geobot. Inst. ETH.
Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics 11: 204-220.
Les DH, Landolt E, Crawford DJ. 1997. Systematics of the Lemnaceae (duckweeds): inferences from micromolecular and morphological data. Plant Systematics and Evolution 204: 161-177.
Li SF, Milliken ON, Pham H, Seyit R, Napoli R, Preston J, Koltunow AM, Parish RW. 2009. The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell 21: 72-89.
Li X, Hou Y, Li M, Zhang F, Yi F, Kang J, Yang Q, Long R. 2022. Overexpression of an ABA-inducible homeodomain-leucine zipper I gene MsHB7 confers salt stress sensitivity to alfalfa. Industrial Crops and Products 177: 114-463.
Lin JY, Le BH, Chen M, Henry KF, Hur J, Hsieh TF, Chen PY, Pelletier JM, Fishcer RL, Harada JJ et al. 2017. Similarity between soybean and Arabidopsis seed methylomes and loss of non-CG methylation does not affect seed development. Proceedings of the National Academy of Sciences, USA 114: 9730-9739.
Liu N-J, Hou L-P, Bao J-J, Wang L-J, Chen X-Y. 2021. Sphingolipid metabolism, transport, and functions in plants: recent progress and future perspectives. Plant Communications 2: 100214.
Liu WX, Liu HL, Qule Q. 2013. Embryo-specific expression of soybean oleosin altered oil body morphogenesis and increased lipid content in transgenic rice seeds. Theoretical and Applied Genetics 126: 2289-2297.
Liu Y, Rosikiewicz W, Pan Z, Jillette N, Wang P, Taghbalaout A, Foox J, Mason C, Caroll M, Cheng A et al. 2021. DNA methylation-calling tools for Oxford Nanopore sequencing: a survey and human epigenome-wide evaluation. Genome Biology 22: 295.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550.
Lutz KA, Wang W, Zdepski A, Michael TP. 2011. Isolation and analysis of high quality nuclear DNA with reduced organellar DNA for plant genome sequencing and resequencing. BMC Biotechnology 11: 54.
Michael T, Bryant D, Gutierrez R, Borisjuk N, Chu P, Zhang H, Xia J, Xia J, Zhou J, Peng H et al. 2017. Comprehensive definition of genome features in Spirodela polyrhiza by high-depth physical mapping and short-read DNA sequencing strategies. The Plant Journal: For Cell and Molecular Biology 89: 617-635.
Michael T, Ernst E, Hartwick N, Chu P, Bryant D, Gilbert S, Ortleb S, Baggs EL, Sree KS, Appenroth KJ et al. 2020. Genome and time-of-day transcriptome of Wolffia australiana link morphological minimization with gene loss and less growth control. Genome Research 31: 225-238.
Morin P Jr, Storey KB. 2009. Mammalian hibernation: differential gene expression and novel application of epigenetic controls. The International Journal of Developmental Biology 53: 433-442.
Oláh V, Hepp A, Mészáros I. 2017. Temporal dynamics in photosynthetic activity of Spirodela polyrhiza turions during dormancy release and germination. Environmental Experimental Botany 136: 50-58.
Persak H, Pitzschke A. 2014. Dominant repression by Arabidopsis transcription factor MYB44 causes oxidative damage and hypersensitivity to abiotic stress. International Journal of Molecular Science 15: 2517-2537.
Rodriguez PL, Benning G, Grill E. 1998. ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Letter 421: 185-190.
Rojas BE, Hartman MD, Figueroa CM, Leaden L, Podesta FE, Iglesias AA. 2019. Biochemical characterization of phosphoenolpyruvate carboxykinases from Arabidopsis thaliana. Biochemical Journal 476: 2939-2952.
Smart CC, Fleming AJ. 1993. A plant gene with homology to d-myo-inositol-3-phosphate synthase is rapidly and spatially up-regulated during an abscisic-acid-induced morphogenic response in Spirodela polyrrhiza. The Plant Journal 4: 279-293.
Smart CC, Trewavas AJ. 1983a. Abscisic acid-induced turion formation in Spirodela polyrrhiza. I. Production and development of the turion. Plant, Cell & Environment 6: 507-514.
Smart CC, Trewavas AJ. 1983b. Abscisic acid-induced turion formation in Spirodela polyrrhiza L. II. Ultrastructure of the turion; a stereological analysis. Plant, Cell & Environment 6: 515-522.
Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR. 2003. Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. The Plant Journal 35: 44-56.
Wan J, Wang R, Zhang P, Sun L, Ju Q, Huang H, Lu S, Tran LS, Xu J. 2021. MYB70 modulates seed germination and root system development in Arabidopsis. iScience 24: 103228.
Wang W, Haberer G, Gundlach H, Glaber C, Nussbaumer T, Luo MC, Lomsadze A, Borodovsky M, Kerstetter RA, Shanklin J et al. 2014a. The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle. Nature Communications 5: 3311.
Wang W, Wu Y, Messing J. 2014b. RNA-Seq transcriptome analysis of Spirodela dormancy without reproduction. BMC Genomics 15: 60.
Wang Z, Wong DCJ, Chen Z, Bai W, Si H, Jin X. 2022. Emerging roles of plant DNA-binding with one finger transcription factors in various hormone and stress signaling pathways. Frontiers in Plant Science 13: 844201.
Watanabe N, Lam E. 2009. Bax Inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants. International Journal of Molecular Science 10: 3149-3167.
Xi W, Liu C, Hou X, Yu H. 2010. MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 22: 1733-1748.
Yang Y, Zhang L, Chen P, Liang T, Li X, Liu H. 2019. UV-B photoreceptor UVR8 interacts with MYB73/MYB77 to regulate auxin responses and lateral root development. EMBO Journal 39: e101928.
Yokochi Y, Yoshida K, Hahn F, Miyagi A, Wakabayashi K, Yamada MK, Weber APM, Hosabori T. 2020. Redox regulation of NADP-malate dehydrogenase is vital for land plants under fluctuating light environment. Proceedings of the National Academy of Sciences, USA 118: e2016903118.
Young MD, Wakefield MJ, Smyth GK, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology 11: 14.
Yu XH, Prakash RR, Sweet M, Shanklin J. 2014. Coexpressing Escherichia coli cyclopropane synthase with Sterculia foetida lysophosphatidic acid acyltransferase enhances cyclopropane fatty acid accumulation. Plant Physiology 164: 455-465.
Zhang W, Xu W, Li S, Zhang H, Liu X, Cui X, Song L, Zhu Y, Chen X, Chen H. 2002. GmAOC4 modulates seed germination by regulating JA biosynthesis in soybean. Theoretical and Applied Genetics 135: 439-434.
Zhao H, Wu D, Kong F, Lin K, Zhang H, Li G. 2017. The Arabidopsis thaliana nuclear factor Y transcription factors. Frontiers in Plant Science 7: 2045.
Zhou A, Liu E, Li H, Feng S, Gong S, Wang J. 2018. PsCor413pm2, a Plasma membrane-localized, cold-regulated protein from Phlox subulata, confers low temperature tolerance in Arabidopsis. International Journal of Molecular Science 19: 2579.