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Seed traits and phylogenomics: prospects for the 21st century

Published online by Cambridge University Press:  06 April 2022

Mariko Nonogaki ,
Satoru Yamazaki ,
Eri Nishiyama ,
Kazuhiko Ohshima  and
Hiroyuki Nonogaki Open the ORCID record for Hiroyuki Nonogaki [Opens in a new window]
Mariko Nonogaki
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
Satoru Yamazaki
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
Eri Nishiyama
Affiliation:
Department of Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga 526-0829, Japan
Kazuhiko Ohshima
Affiliation:
Department of Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga 526-0829, Japan
Hiroyuki Nonogaki
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
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Abstract

Genetic and biochemical studies have greatly advanced our understanding of the biology of seeds in recent years. Another area of study, which could accelerate contemporary seed biology research, is phylogenomics that integrates the wealth of genome sequence data with evolutionary biology. The recent phylogenomic study of the DELAY OF GERMINATION1 family genes exemplifies how the molecular evolution of seed genes can be traced back through early diverging plants and what implications can be obtained from the analysis of seed gene diversification at ancient times. The identification of possible ancestors of seed genes in non-seed plants could illuminate the ancient roots of the molecular mechanisms driving seed maturation programmes. It is possible that the origins of molecular mechanisms associated with the induction of seed storage proteins and desiccation tolerance proteins date back to the time of, or even prior to, early diverging land plants. Abscisic acid-dependent growth arrest or dormancy mechanisms might date back to red algae, one of the oldest algal groups. Thus, understanding algal cell biology will also be an integral part of future seed biology research. Unravelling key events associated with the evolution of seed- and non-seed plants will not only advance basic research but could also contribute to applied aspects of seed science, potentially leading to technology development for agriculture.

Keywords

DOG1DOG1-LIKEdormancyevolutiongerminationperspectivesphylogenomics
Type
Research Opinion
Information
Seed Science Research , Volume 32 , Special Issue 3: Seed Innovation Systems for the 21st Century , September 2022 , pp. 137 - 143
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Bentsink, L, Jowett, J, Hanhart, CJ and Koornneef, M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences USA 103, 17042–17047.CrossRefGoogle ScholarPubMed
Cheng, S, Xian, W, Fu, Y, Marin, B, Keller, J, Wu, T, Sun, W, Li, X, Xu, Y, Zhang, Y, Wittek, S, Reder, T, Günther, G, Gontcharov, A, Wang, S, Li, L, Liu, X, Wang, J, Yang, H, Xu, X, Delaux, PM, Melkonian, B, Wong, GKS and Melkonian, M (2019) Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179, 1057–1067.CrossRefGoogle ScholarPubMed
Cutler, SR, Rodriguez, PL, Finkelstein, RR and Abrams, SR (2010) Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651–679.CrossRefGoogle ScholarPubMed
Cyrek, M, Fedak, H, Ciesielski, A, Guo, YW, Sliwa, A, Brzezniak, L, Krzyczmonik, K, Pietras, Z, Kaczanowski, S, Liu, FQ and Swiezewski, S (2016) Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1. Plant Physiology 170, 947–955.CrossRefGoogle ScholarPubMed
Dekkers, BJW, He, H, Hanson, J, Willems, LAJ, Jamar, DCL, Cueff, G, Rajjou, L, Hilhorst, HWM and Bentsink, L (2016) The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. The Plant Journal 85, 451–465.CrossRefGoogle ScholarPubMed
de Vries, J and Archibald, JM (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytologist 217, 1428–1434.CrossRefGoogle ScholarPubMed
de Vries, J, Curtis, BA, Gould, SB and Archibald, JM (2018) Embryophyte stress signaling evolved in the algal progenitors of land plants. Proceedings of the National Academy of Sciences USA 115, E3471–E3480.CrossRefGoogle ScholarPubMed
Eklund, DM, Kanei, M, Flores-Sandoval, E, Ishizaki, K, Nishihama, R, Kohchi, T, Lagercrantz, U, Bhalerao, RP, Sakata, Y and Bowman, JL (2018) An evolutionarily conserved abscisic acid signaling pathway regulates dormancy in the liverwort Marchantia polymorpha. Current Biology 28, 3691–3699.CrossRefGoogle ScholarPubMed
Fedak, H, Palusinska, M, Krzyczmonik, K, Brzezniak, L, Yatusevich, R, Pietras, Z, Kaczanowski, S and Swiezewski, S (2016) Control of seed dormancy in Arabidopsis by a cis-acting noncoding antisense transcript. Proceedings of the National Academy of Sciences USA 113, E7846–E7855.CrossRefGoogle ScholarPubMed
Feng, X, Holzinger, A, Permann, C, Anderson, D and Yin, Y (2021) Characterization of two Zygnema strains (Zygnema circumcarinatum SAG 698-1a and SAG 698-1b) and a rapid method to estimate nuclear genome size of Zygnematophycean green algae. Frontiers in Plant Science 12, 103.CrossRefGoogle Scholar
Fogliani, B, Gâteblé, G, Villegente, M, Fabre, I, Klein, N, Anger, N, Baskin, CC and Scutt, CP (2017) The morphophysiological dormancy in Amborella trichopoda seeds is a pleisiomorphic trait in angiosperms. Annals of Botany 119, 581–590.Google ScholarPubMed
Friedman, WE (2008) Hydatellaceae are water lilies with gymnospermous tendencies. Nature 453, 94–97.CrossRefGoogle ScholarPubMed
Gitzendanner, MA, Soltis, PS, Wong, GK-S, Ruhfel, BR and Soltis, DE (2018) Plastid phylogenomic analysis of green plants: a billion years of evolutionary history. American Journal of Botany 105, 291–301.CrossRefGoogle ScholarPubMed
González-Morales, SI, Chávez-Montes, RA, Hayano-Kanashiro, C, Alejo-Jacuinde, G, Rico-Cambron, TY, de Folter, S and Herrera-Estrella, L (2016) Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 113, E5232–E5241.CrossRefGoogle ScholarPubMed
Graeber, K, Voegele, A, Büttner-Mainik, A, Sperber, K, Mummenhoff, K and Leubner-Metzger, G (2013) Spatiotemporal seed development analysis provides insight into primary dormancy induction and evolution of the Lepidium DELAY OF GERMINATION1 genes. Plant Physiology 161, 1903–1917.CrossRefGoogle ScholarPubMed
Graeber, K, Linkies, A, Steinbrecher, T, Mummenhoff, K, Tarkowská, D, Turečková, V, Ignatz, M, Sperber, K, Voegele, A, de Jong, H, Urbanova, T, Strnad, M and Leubner-Metzger, G (2014) DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination. Proceedings of the National Academy of Sciences USA 111, E3571–E3580.CrossRefGoogle ScholarPubMed
Hori, K, Maruyama, F, Fujisawa, T, Togashi, T, Yamamoto, N, Seo, M, Sato, S, Yamada, T, Mori, H, Tajima, N, Moriyama, T, Ikeuchi, M, Watanabe, M, Wada, H, Kobayashi, K, Saito, M, Masuda, T, Sasaki-Sekimoto, Y, Mashiguchi, K, Awai, K, Shimojima, M, Masuda, S, Iwai, M, Nobusawa, T, Narise, T, Kondo, S, Saito, H, Sato, R, Murakawa, M, Ihara, Y, Oshima-Yamada, Y, Ohtaka, K, Satoh, M, Sonobe, K, Ishii, M, Ohtani, R, Kanamori-Sato, M, Honoki, R, Miyazaki, D, Mochizuki, H, Umetsu, J, Higashi, K, Shibata, D, Kamiya, Y, Sato, N, Nakamura, Y, Tabata, S, Ida, S, Kurokawa, K and Ohta, H (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications 5, 2–6.CrossRefGoogle ScholarPubMed
Khanday, I and Sundaresan, V (2021) Plant zygote development: recent insights and applications to clonal seeds. Current Opinion in Plant Biology 59, 101993.CrossRefGoogle Scholar
Kim, BH, Li, K, Kim, J-T, Park, Y, Jang, H, Wang, X, Xie, Z, Won, SM, Yoon, H-J, Lee, G, Jang, WJ, Lee, KH, Chung, TS, Jung, YH, Heo, SY, Lee, Y, Kim, J, Cai, T, Kim, Y, Prasopsukh, P, Yu, Y, Yu, X, Avila, R, Luan, H, Song, H, Zhu, F, Zhao, Y, Chen, L, Han, SH, Kim, J, Oh, SJ, Lee, H, Lee, CH, Huang, Y, Chamorro, LP, Zhang, Y and Rogers, JA (2021) Three-dimensional electronic microfliers inspired by wind-dispersed seeds. Nature 597, 503–510.CrossRefGoogle ScholarPubMed
Kobayashi, Y, Ando, H, Hanaoka, M and Tanaka, K (2016) Abscisic acid participates in the control of cell cycle initiation through heme homeostasis in the unicellular red alga Cyanidioschyzon merolae. Plant and Cell Physiology 57, 953–960.CrossRefGoogle ScholarPubMed
Mattana, E, Ulian, T and Pritchard, HW (2021) Seeds as natural capital. Trends Plant Science 27, 139–146.CrossRefGoogle ScholarPubMed
Née, G, Kramer, K, Nakabayashi, K, Yuan, B, Xiang, Y, Miatton, E, Finkemeier, I and Soppe, WJJ (2017) DELAY of GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nature Communications 8, 72.CrossRefGoogle ScholarPubMed
Nishimura, N, Tsuchiya, W, Moresco, JJ, Hayashi, Y, Satoh, K, Kaiwa, N, Irisa, T, Kinoshita, T, Schroeder, JI, Yates, JR, Hirayama, T and Yamazaki, T (2018) Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nature Communications 9, 2132.CrossRefGoogle Scholar
Nishiyama, T, Sakayama, H, de Vries, J, Buschmann, H, Saint-Marcoux, D, Ullrich, KK, Haas, FB, Vanderstraeten, L, Becker, D, Lang, D, Vosolsobě, S, Rombauts, S, Wilhelmsson, PKI, Janitza, P, Kern, R, Heyl, A, Rümpler, F, Villalobos, LIAC, Clay, JM, Skokan, R, Toyoda, A, Suzuki, Y, Kagoshima, H, Schijlen, E, Tajeshwar, N, Catarino, B, Hetherington, AJ, Saltykova, A, Bonnot, C, Breuninger, H, Symeonidi, A, Radhakrishnan, GV, Nieuwerburgh, FV, Deforce, D, Chang, C, Karol, KG, Hedrich, R, Ulvskov, P, Glöckner, G, Delwiche, CF, Petrášek, J, Van de Peer, Y, Friml, J, Beilby, M, Dolan, L, Kohara, Y, Sugano, S, Fujiyama, A, Delaux, PM, Quint, M, Theißen, G, Hagemann, M, Harholt, J, Dunand, C, Zachgo, S, Langdale, J, Maumus, F, Van Der Straeten, D, Gould, SB and Rensing, SA (2018) The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174, 448–464.CrossRefGoogle ScholarPubMed
Nishiyama, E, Nonogaki, M, Yamazaki, S, Nonogaki, H and Ohshima, K (2021) Ancient and recent gene duplications as evolutionary drivers of the seed maturation regulators DELAY OF GERMINATION1 family genes. New Phytologist 230, 889–901.CrossRefGoogle ScholarPubMed
Nonogaki, H (2019) The long-standing paradox of seed dormancy unfolded? Trends in Plant Science 24, 989–998.CrossRefGoogle ScholarPubMed
Nonogaki, H (2020) A repressor complex silencing ABA signaling in seeds? Journal of Experimental Botany 71, 2847–2853.CrossRefGoogle ScholarPubMed
Nonogaki, H, Nishiyama, E, Ohshima, K and Nonogaki, M (2020) Ancient memories of seeds: aBA-dependent growth arrest and reserve accumulation. Trends in Genetics 36, 464–473.CrossRefGoogle ScholarPubMed
Povilus, RA, Losada, JM and Friedman, WE (2015) Floral biology and ovule and seed ontogeny of Nymphaea thermarum, a water lily at the brink of extinction with potential as a model system for basal angiosperms. Annals of Botany 115, 211–226.CrossRefGoogle Scholar
Sall, K, Dekkers, BJW, Nonogaki, M, Katsuragawa, Y, Koyari, R, Hendrix, D, Willems, LAJ, Bentsink, L and Nonogaki, H (2019) DELAY OF GERMINATION 1-LIKE 4 acts as an inducer of seed reserve accumulation. The Plant Journal 100, 7–19.CrossRefGoogle ScholarPubMed
Shinozawa, A, Otake, R, Takezawa, D, Umezawa, T, Komatsu, K, Tanaka, K, Amagai, A, Ishikawa, S, Hara, Y, Kamisugi, Y, Cuming, AC, Hori, K, Ohta, H, Takahashi, F, Shinozaki, K, Hayashi, T, Taji, T and Sakata, Y (2019) SnRK2 protein kinases represent an ancient system in plants for adaptation to a terrestrial environment. Communications Biology 2, 30.CrossRefGoogle ScholarPubMed
Sun, Y, Harpazi, B, Wijerathna-Yapa, A, Merilo, E, de Vries, J, Michaeli, D, Gal, M, Cuming, AC, Kollist, H and Mosquna, A (2019) A ligand-independent origin of abscisic acid perception. Proceedings of the National Academy of Sciences USA 116, 24892–24899.CrossRefGoogle ScholarPubMed
Watanabe, S, Hanaoka, M, Ohba, Y, Ono, T, Ohnuma, M, Yoshikawa, H, Taketani, S and Tanaka, K (2013) Mitochondrial localization of ferrochelatase in a red alga Cyanidioschyzon merolae. Plant and Cell Physiology 54, 1289–1295.CrossRefGoogle Scholar
Wickett, NJ, Mirarab, S, Nguyen, N, Warnow, T, Carpenter, E, Matasci, N, Ayyampalayam, S, Barker, MS, Burleigh, JG, Gitzendanner, MA, Ruhfel, BR, Wafula, E, Der, JP, Graham, SW, Mathews, S, Melkonian, M, Soltis, DE, Soltis, PS, Miles, NW, Rothfels, CJ, Pokorny, L, Shaw, AJ, DeGironimo, L, Stevenson, DW, Surek, B, Villarreal, JC, Roure, B, Philippe, H, dePamphilis, CW, Chen, T, Deyholos, MK, Baucom, RS, Kutchan, TM, Augustin, MM, Wang, J, Zhang, Y, Tian, Z, Yan, Z, ei Wu, X, Sun, X, Wong, GKS and Leebens-Mack, J (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences USA 111, E4859–E4868.CrossRefGoogle ScholarPubMed
Wodniok, S, Brinkmann, H, Glöckner, G, Heidel, AJ, Philippe, H, Melkonian, M and Becker, B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evolutionary Biology 11, 104.CrossRefGoogle ScholarPubMed
Xu, W, Fiume, E, Coen, O, Pechoux, C, Lepiniec, L and Magnani, E (2016) Endosperm and nucellus develop antagonistically in Aarabidopsis seeds. The Plant Cell 28, 1343–1360.CrossRefGoogle Scholar
Yu, C, Qiao, G, Qiu, W, Yu, D, Zhou, S, Shen, Y, Yu, G, Jiang, J, Han, X, Liu, M, Zhang, L, Chen, F, Chen, Y and Zhuo, R (2018) Molecular breeding of water lily: engineering cold stress tolerance into tropical water lily. Horticulture Research 5, 73.CrossRefGoogle ScholarPubMed