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Florigen Revisited: Proteins of the FT/CETS/PEBP/PKIP/Ybhb Family

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Florigen Revisited: Proteins of the FT/CETS/PEBP/PKIP/Ybhb Family bioRxiv preprint doi: https://doi.org/10.1101/2021.04.16.440192; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 1 Breakthrough Report 2 3 Florigen revisited: proteins of the FT/CETS/PEBP/PKIP/YbhB family may be the enzymes 4 of small molecule metabolism 5 6 Short title: Florigen-family proteins may be enzymes 7 8 Olga Tsoy1,4 and Arcady Mushegian2,3* 9 10 11 1 Chair of Experimental Bioinformatics, TUM School of Life Sciences Weihenstephan, Technical 12 University of Munich (TUM), 3, Maximus-von-Imhof-Forum, Freising, 85354, Germany 13 14 2 Molecular and Cellular Biology Division, National Science Foundation, 2415 Eisenhower 15 Avenue, Alexandria, Virginia 22314, USA 16 17 3 Clare Hall College, University of Cambridge, Cambridge CB3 9AL, United Kingdom 18 19 4 current address: Chair of Computational Systems Biology, University of Hamburg, 20 Notkestrasse, 9, 22607, Hamburg, Germany 21 22 * corresponding author: [email protected] 23 24 25 26 27 The author responsible for distribution of materials integral to the findings presented in this 28 article in accordance with the policy described in the Instructions for Authors 29 (www.plantcell.org) is Arcady Mushegian ([email protected]). 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.16.440192; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 30 Abstract 31 Flowering signals are sensed in plant leaves and transmitted to the shoot apical meristems, where 32 the formation of flowers is initiated. Searches for a diffusible hormone-like signaling entity 33 (“florigen”) went on for many decades, until in the 1990s a product of plant gene FT was 34 identified as the key component of florigen, based on genetic evidence and protein localization 35 studies. Sequence homologs of FT protein are found throughout prokaryotes and eukaryotes; 36 some eukaryotic family members appear to bind phospholipids or interact with the components 37 of the signal transduction cascades. We studied molecular features of the FT homologs in 38 prokaryotes and analyzed their genome context, to find tentative evidence connecting the 39 bacterial family members with small molecule metabolism, often involving sugar- or 40 ribonucleoside-containing substrates. Most FT homologs share a constellation of five charged 41 residues, three of which, i.e., two histidines and an aspartic acid, circumfere the rim of a well- 42 defined cavity on the protein surface. We argue that this conserved feature is more likely to be an 43 enzymatic active center than a catalytically inactive ligand-binding site. We propose that most of 44 FT-related proteins are enzymes operating on small diffusible molecules, which may constitute 45 an overlooked essential ingredient of the florigen signal. 46 47 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.16.440192; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 48 Introduction 49 Flower production in plants occurs in response to the environmental cues – most 50 importantly, changes in the day length. The role of photoperiodicity in all living forms from 51 bacteria to higher eukaryotes is well established, and it has been shown in numerous studies that 52 the perception of the photoperiodic signal in plants occurs primarily in the leaves. Flowers, 53 however, are formed mostly by shoot apical meristems (SAM), which are typically shielded from 54 direct light, and the mechanisms which convey the flowering signal from leaves to SAMs have 55 been a matter of speculation and investigation for most of the 20th century. 56 Plant physiologists have established, by the 1930s, that angiosperms generally fall in 57 three categories, i.e., long-day plants, in which blooming is turned on by day lengthening / night 58 shortening; short-day plants, which initiate blooming upon day shortening / night lengthening; 59 and day-neutral plants, which bloom in response to the cues other than day length (Garner and 60 Allard, 1920; Knott, 1934). Experiments on flowering in partially shaded plants and in grafts 61 between light-induced and uninduced plants suggested the existence of a flower-promoting 62 diffusible substance; the idea may have been first proposed by Julius Sachs (Sachs, 1865), but 63 was consolidated in the modern form by M. Chailakhyan (1902-1991), who proposed the term 64 “florigen” as the name for the flower-inducing chemical entity (Chailakhyan, 1936). The early 65 research on the photoperiodic signal sensing in leaves is reviewed in (Zeevaart, 2006; 66 Kobayashi and Weigel, 2007), and an account of Chailakhyan's remarkable life and research 67 work can be found in (Romanov, 2012). 68 The transfer of a flowering signal from leaves to the shoot apex has been studied over the 69 years in many species of flowering plants, and general similarity of its properties to those of 70 small molecules was noted; for example, the florigen fraction appeared to move in phloem at the 71 speed comparable to that of other plant assimilates (King et al., 1968). It has been established 72 also that grafts and extracts of induced plants could transfer flowering ability not only in the 73 uninduced vegetatively developing plants of the same species, but sometimes also in other 74 species or genera, suggesting the evolutionary conservation of the signaling pathways (Zeevaart, 75 1976). 76 Despite general acceptance of the idea of florigen as a conserved hormone-like substance, 77 the attempts at the isolation and chemical characterization of the responsible entity did not 78 succeed for several decades. Reviewing the state of the affairs in 1976, J.A.D. Zeewart listed the 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.16.440192; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 79 factors that have been tested unsuccessfully for the ability to induce plant flowering; the list of 80 failed candidates included sugars, amino acids, sterols, gibberellins, salicylic acid, ethylene, 81 cytokinins, the photosynthetic capacity, initiation of protein synthesis, and others (Zeevaart, 82 1976). Several hypotheses have been put forward to explain the difficulties of identifying 83 florigen: perhaps it was not one molecule but several distinct hormones or metabolites, acting 84 jointly in a specific succession, or as a mix with specific ratio of components; or, possibly, the 85 identity of florigen was masked by simultaneous presence of flowering inhibitors in the same 86 samples (Lang et al., 1977); or, maybe, flowering was caused by propagation of electric, rather 87 than chemical, signals between leaves and meristems, such as plasma membrane potential (Penel 88 et al., 1985). 89 Despite all the work to test these and other hypotheses, there was little progress in 90 biochemical characterization of florigen until early 1990s, when the search for a flower-inducing 91 activity started employing the tools of molecular biology. For example, in what may have been 92 the last published study by Chailakhyan, a radiolabeled protein band of ~27 kDa was observed in 93 the induced, but not in naïve, leaves of Rudbeckia, followed by accumulation of the similar-sized 94 band in the shoot apex tissues (Milyaeva et al., 1991); the work is largely unavailable to the 95 Western reader because of the temporary interruption of translation and indexing of Russian- 96 language journals upon the collapse of the Soviet Union. Around the same time, it has been 97 shown (Takeba et al., 1990) that aqueous extracts of Lemna, Pharbitis and Brassica contained a 98 flower-inducing fraction dominated by a 20-30 kDa protein band; the authors noted, however, 99 that the florigen activity was resistant to proteinase K digestion that removed the protein, perhaps 100 suggesting a role for an associated small molecule. 101 Nearly simultaneously, the results of genetic screens for A.thaliana mutants with late 102 flowering phenotypes were published (Koornneef et al., 1991). This was a watershed moment in 103 the studies of the molecular determinants of flowering initiation, and the important discoveries 104 that ensued in the following three decades have been reviewed extensively (Andrés and 105 Coupland, 2012; Lifschitz et al., 2014; Kinoshita and Richter, 2020). The state of the knowledge 106 may be summarized as follows. 107 Flowering in Arabidopsis is LD-dependent, and is enabled through the circadian clock- 108 controlled transcriptional co-regulator CONSTANS (CO) and its target FLOWERING LOCUS T. 109 The protein product of the latter gene has emerged as the integrator of the environmental inputs, 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.16.440192; this version posted April 16, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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