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Review
. 2024 May 1;36(5):1334-1357.
doi: 10.1093/plcell/koae044.

Reflections on the ABC model of flower development

John L Bowman  1   2 , Edwige Moyroud  3   4
Affiliations
Review

Reflections on the ABC model of flower development

John L Bowman et al. Plant Cell. .

Abstract

The formulation of the ABC model by a handful of pioneer plant developmental geneticists was a seminal event in the quest to answer a seemingly simple question: how are flowers formed? Fast forward 30 years and this elegant model has generated a vibrant and diverse community, capturing the imagination of developmental and evolutionary biologists, structuralists, biochemists and molecular biologists alike. Together they have managed to solve many floral mysteries, uncovering the regulatory processes that generate the characteristic spatio-temporal expression patterns of floral homeotic genes, elucidating some of the mechanisms allowing ABC genes to specify distinct organ identities, revealing how evolution tinkers with the ABC to generate morphological diversity, and even shining a light on the origins of the floral gene regulatory network itself. Here we retrace the history of the ABC model, from its genesis to its current form, highlighting specific milestones along the way before drawing attention to some of the unsolved riddles still hidden in the floral alphabet.

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Conflict of interest statement

Conflict of interest statement. None declared.

Figures

Figure 1.
Figure 1.
Early descriptions of flower variants. A) Single- (left) and double-flowered (right) wallflowers, Erysimum cheiri (Gerard et al. 1597). B) An apple mutant in which the petals are transformed to another whorl of sepals and the stamens are transformed into carpels. This tree was used for cross-fertilization, where “the ladies and young girls of Saint-Valery compete to ‘make their apple’ [that's the expression they use]. A hermaphrodite flower, picked in dry weather from any apple tree, is applied to each flower and left there until fertilization is completed and it falls off naturally. Then a ribbon of colour is attached to the fertilized bouquet so that, when autumn comes, each person can recognize the fruit created by their own hand” (Tillette de Clermont-Tonnere 1825). C) An apetala2-1 pistillata-1 agamous-1 flower consisting of an indeterminate number of whorls of leaf-like organs. (A,B, Biodiversity Heritage Library; C, photo, J.L.B.).
Figure 2.
Figure 2.
The ABC model and mutant phenotypes on which it is based. A) Wild-type Arabidopsis flower (left) and floral diagram (right). se, sepal; pe, petal; st, stamen; ca, carpel; floral structure: se, pe, st, ca. B) Early version of the ABC model from mid-1988. C) ABC model in its current incarnation; the ABC activities are whorl specific while those of SEPALLATA are throughout the flower. “Dimers of dimers,” or quartets, of MIKCC-type MADS box proteins determine organ identity. D) Early expression of the ABC genes mapped onto developing flowers. E)apetala2-1: floral structure: le (leaf), pe, st, ca. F)apetala2-2: floral structure: ca, missing, st, ca. G)apetala3-1: floral structure: se, se, ca, ca. H)pistillata-1. floral structure: se, se, ca (most fused with the central carpels), ca. I)agamous-1: floral structure: (se, pe, pe)n—the flower meristem is indeterminate with the organs repeating. J)apetala2-2 pistillata-1: floral structure: ca, missing, missing, ca—in some cases all organs are fused into a single structure. K)apetala3-1 agamous-1: floral structure: (se, se, se)n. L)apetala2-2 agamous −1: floral structure: (le/ca (carpelloid leaf), st/pe (stamenoid petal), st/pe)n. M)apetala2-2 pistillata-1 agamous-1: floral structure: (le/ca (carpelloid leaf), le/ca, le/ca)n. All photos by J.L.B.; A (Lee et al. 2005b); D, F, H, J, L, M (Bowman 2001; copyright 2001, John Wiley & Sons, Ltd., reproduced with permission); G (Bowman et al. 1989); K (Bowman et al. 1991; copyright 1991, Company of Biologists, reproduced with permission).
Figure 3.
Figure 3.
Molecular and genetic extensions of the ABC model. A) Low stringency Southern blot using AGAMOUS as a probe on Arabidopsis DNA cut with EcoRI. B) Simplified MADS-box gene phylogeny: A-class, red; B-class, yellow; C-class, blue; E-class, grey; gymnosperm sequences, purple; fern sequences, pink. In both B and C clades, additional angiosperm paralogs are present and often have functions related to the B and C-class genes. Gymnosperm orthologs exist (or existed) for all classes, and the split between the B-class and A/C/E classes occurred in the common ancestor of euphyllophytes. The MIKCC protein structure is indicated at the bottom; MADS, DNA binding domain; I, intervening domain; K, keratin-related domain; C, carboxyl terminal domain. C)35S:APETALA3; 35S:PISTILLATA: floral structure: pe, pe, st, st. D)sepallata123: floral structure: (se, se, se)n. E)35S:AG/PI/AP3/SEP3: floral structure: (st, st, st)n; leaves are transformed into stamens. F)35S:PI/AP3/SEP3: leaves, but not cotyledons, are transformed into petals. G)apetala2-2 pistillata-1 agamous-1 shatterproof12: floral structure: (le, le, le)n. H)apetala1-1: floral structure: br (bract-like), pe (or missing), st, ca; first whorl bracts may also have flower meristem in their axils, and ectopic flower meristems can arise. The photo depicts a “single” basal flower, with later produced flowers having decreasing indeterminacy. I)apetala1-5: floral structure: br (or br/ca), pe (or pe/st), st, ca. this flower has both a stamenoid petal (pe/st) and carpel (ca) tissue at the margin of a first whorl bract. J)apetala1-1 cauliflower-1: when grown in nonfloral inductive conditions, what should have been a flower is only a collection of inflorescence meristems that reiterate a spiral initiation pattern (lower panel). K) Additional whorls of stamens (4) develop interior to the third whorl (3) in superman flowers; floral structure: se, pe, st, st, (st). L) Flowers of superman agamous double mutants have an outer whorl of sepals and an indeterminate number of whorls of petals; floral structure: se, pe, pe, pe, etc. E-F courtesy of Koji Goto; all other photos by JLB except G by Ji-Young Lee; C (Bowman 2001; copyright 2001, John Wiley & Sons, Ltd., reproduced with permission); D, G (Lee et al. 2005b); I (Bowman et al. 1993; copyright 1993, Company of Biologists, reproduced with permission).
Figure 4.
Figure 4.
Parallels of developmental gene network architectures. Patterning of pair-rule genes expression [such as Even-skipped (Eve) and Fushi tarazu (Ftz)] along the antero-posterior axis of the fly body involves the induction of broad overlapping expression domains by various combination of upstream regulators (GAP genes) at early stages, followed by establishment of discreet stripes through cross-regulation between the different pair-rule genes. Similarly, the overlapping expression domains of ABC genes are refined through the action of positive feedback (i.e. between APETALA3 (AP3) and PISTILLATA (PI) B class genes) and cross inhibition (i.e. between A and C class genes). Feedforward loops are also common regulatory motifs to control the timing of events patterning the fly body or the floral meristem of Arabidopsis: in Drosophila, maternal determinants such as Bicoid activate the expression of Hunchback and together they pattern GAP gene expression. In Arabidopsis LFY promotes APETALA1 (AP1) transcription during floral induction, which inhibits expression of SEPALLATA3 repressors (AGL24/SVP/SOC1), preventing precocious expression of B and C class genes. LEAFY and UNUSUAL FLORAL ORGAN (UFO) physically interact (Chae et al. 2008); but whether the partnerships LEAFY—WUSCHEL (WUS) and LEAFY—unknown factor (?) that regulate the expression of A and C class genes respectively also require direct protein-protein interaction remains unclear (Lohmann et al. 2001; Zhao et al. 2018). Se, sepal; Pe, petal, St, stamen; Ca, carpel.
Figure 5.
Figure 5.
Evolutionary conservation of the ABC model and its variants. A) The outermost whorl of grass flowers is occupied by the palea (p) and lemma (l) and the second whorl by lodicules, which swell to facilitate flower opening. B) The outer 2 whorls of tulips are tepals, which are petal-like, and B-class gene expression is in all whorls except the innermost carpels. C) A proliferation of APETALA3 paralogs have sub- and neofunctionalized to produce 3 distinct compositions of B-class, with 1 set promoting the development of staminodes (sd), modified stamen-like organs that may act to deter herbivory (Hodges and Tucker 2005). D) Orchid also possesses a proliferation of APETALA3 paralogs that act in combination to promote differentiation of the outer tepals (ot), inner lateral tepals (ilt), and labellum (la) that comprise the perianth. E) The capitulum of Asteraceae consists of central disc florets (df) and peripheral ray florets (rf), with the fertile disc florets developing a conspicuous pappus ring (p), homologous with sepals, in their outer whorls. F) In some species, organ identity transitions may not be abrupt, such as with petal and stamen identity in Opuntia. G)Lacandonia schismatica is the only angiosperm where the order of organs is transposed, with stamens (st) developing interior to carpels (ca). L. schismatica plants (arrow) grow on the Lacandon jungle floor, are small (10 cm), achlorophyllous, and saprophytic. H) Pines have separate male and female cones, with C-class being expressed in both and B-class limited to male cones. SEM of L. schismatica courtesy of Barbara Ambrose; all other photos by J.L.B.
Figure 6.
Figure 6.
Paralog sub- and neofunctionalization generates diversity. Paralogs of A/E (AGL6-1, AGL6-2) and B (AP3-1, AP3-2) class genes in orchids have acquired distinct expression patterns, allowing the formation of different quartets across the perianth. This “P code” (Hsu et al. 2015) can explain the activation of different targets genes in different organs within a whorl (i.e. lateral petals vs. lip) or even between different part of the same organ (lower and upper region of the lateral petals): the SP and L” complexes comprise a dimer of AP3-1 (light blue) combines with a dimer of AGL6-1 (purple) or AGL6-2 (red) respectively. Those can bind to promoters harboring distinct CArG box shape, spacing, and orientation, allowing the 2 quartets to regulate different morphological features. The SP complex can trigger uniform pigment production across the petal/sepal epidermis while L” induces spot formation and promotes the production of flat epidermis cells associated with a curvature of the lower lateral petal region (Photo, modified from Zygomorf1 by Christer Johansson via Wikimedia Commons https://creativecommons.org/licenses/by-sa/3.0/).
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