SUPERMAN strikes again in legumes

Abstract

The SUPERMAN (SUP) gene was described in Arabidopsis thaliana over 30 years ago. SUP was classified as a cadastral gene required to maintain the boundaries between reproductive organs, thus controlling stamen and carpel number in flowers. We summarize the information on the characterization of SUP orthologs in plant species other than Arabidopsis, focusing on the findings for the MtSUP, the ortholog in the legume Medicago truncatula. M. truncatula has been widely used as a model system to study the distinctive developmental traits of this family of plants, such as the existence of compound inflorescence and complex floral development. MtSUP participates in the complex genetic network controlling these developmental processes in legumes, sharing conserved functions with SUP. However, transcriptional divergence between SUP and MtSUP provided context-specific novel functions for a SUPERMAN ortholog in a legume species. MtSUP controls the number of flowers per inflorescence and the number of petals, stamens and carpels regulating the determinacy of ephemeral meristems that are unique in legumes. Results obtained in M. truncatula provided new insights to the knowledge of compound inflorescence and flower development in legumes. Since legumes are valuable crop species worldwide, with high nutritional value and important roles in sustainable agriculture and food security, new information on the genetic control of their compound inflorescence and floral development could be used for plant breeding.

Keywords: Medicago truncatula; MtSUP; SUPERMAN; compound inflorescence; flower development; flower number; legumes.

Figure 1

Comparative floral development of Arabidopsis thaliana and Medicago truncatula. (A) Comparative schematic representation among superman (sup) mutant alleles in Arabidopsis regarding floral organ number. Wild type A. thaliana flower: 4 sepals, 4 petals, 6 stamens and two fused carpels. (B) Comparative schematic representation among superman (mtsup) mutant alleles in Medicago regarding floral organ number. Wild type M. truncatula flower: 5 sepals, 5 petals, 10 stamens, 9 fused (staminal tube) and one free, and a single carpel. In Arabidopsis, the ‘superman’ class of mutants harbors supernumerary stamens and reduced or absent carpel, resembling mtsup-2 showing additional petals at the expense of stamens. An increased number of carpels characterize the “superwoman” class. Similar phenotypes displayed the mtsup-1 (class 2 and 3) alleles, with two or three carpels in M. truncatula. The “supersex” class, to which sup-5 allele belong, produces more stamens and additional carpels. This phenotype is observed in mtsup-1 allele (class 4). Also, additional petals are produced by this allele. (C) Left. In A. thaliana organ differentiation is centripetal and sequential. First are differentiated the sepal primordia, then the petal primordia, the stamen primordia and finally the carpel primordium. Right. In M. truncatula, the four common primordia differentiate petals and stamens in W2 and W3 respectively. (D) Floral meristem of M. truncatula showing the early carpel primordium (C, green) in the centre, the four common primordia (CP, orange) and the sepal primordia (S). (E) Each common primordium differentiates petals (P, yellow) in W2 and antepetal (Stp) and antesepal (Sts) stamens in W3 (orange). VM, vegetative meristem; FM, floral meristem; I1, primary inflorescence meristem; I2, secondary inflorescence meristem; spk, spike; S, sepal primordium; CP, common primordium; P, petal primordium; St, stamen primordium; C, carpel primordium. Scale bars, 25 μm in (D, E) Adapted from Benlloch et al., 2003; Breuil-Broyer et al., 2016; Prunet et al., 2017 and Rodas et al., 2021.

Figure 2

MtSUP controls compound inflorescence development in M. truncatula. (A) MtSUP transcript is firstly detected in the I2. (B) Later on MtSUP activity is detected in the FM. (C) During early floral development MtSUP expression is detected in the common primordia (CP). (D) MtFULc expression in the wild type (WT) flower. (E) MtFULc expression in the mtsup-1 mutant. MtFULc transcript occupies a wider area in MtSUP mutants compared to the WT. (F) Schematic representation of the compound inflorescence development in Medicago with the formation of an I2 and the terminal spike in the WT and a new FM instead the spike in the mtsup-1 mutant. (G) SEM image of a WT floral primordium with its respective bract and spike. (H) The WT of M. truncatula R108 produces one or two flowers per inflorescence and terminates in a spike. (I) In mtsup-1, the I2* (future spike) acquires floral identity. (J) In the mtsup-1 mutant the residual cells of the I2 terminate as a new flower (F*) instead a spike. (K) Comparative schematic representation of SUP and MtSUP expression patterns during inflorescence and flower development in Arabidopsis and Medicago. SUP and MtSUP are orthologs that have functionally diverged through changes in their gene transcription patterns. IM, inflorescence meristem; I1, primary inflorescence meristem; I2, secondary inflorescence meristem; FM, floral meristem; CP, common primordium; S, sepal primordium; P, petal primordium; C, carpel primordium; Br, bract; Spk, spike; F*, new flower. Scale bars, 20 μm in (G, I), and 2 mm in (H, J) Adapted from Rodas et al. (2021).