The TM5 MADS Box Gene Mediates Organ Differentiation in the Three Inner Whorls of Tomato Flowers.

Abstract

The tomato MADS box gene no. 5 (TM5) is shown here to be expressed in meristematic domains fated to form the three inner whorls-petals, stamens, and gynoecia-of the tomato flower. TM5 is also expressed during organogenesis and in the respective mature organs of these three whorls. This is unlike the major organ identity genes of the MADS box family from Antirrhinum and Arabidopsis, which function in overlapping primordial territories consisting of only two floral whorls each. The developmental relevance of the unique expression pattern of this putative homeotic gene was examined in transgenic plants. In agreement with the expression patterns, antisense RNA of the TM5 gene conferred both early and late alterations of morphogenetic markers. Early defects consist of additional whorls or of a wrong number of organs per whorl. Late, organ-specific changes include evergreen, cauline, and unabscised petals; green, dialytic, and sterile anthers; and sterile carpels and defective styles on which glandular trichomes characteristic of sepals and petals are ectopically formed. However, a complete homeotic transformation of either organ was not observed. The early and late floral phenotypes of TM5 antisense plants suggest that TM5 mediates two unrelated secondary regulatory systems. One system is the early function of the floral meristem identity genes, and the other system is the function of the major floral organ identity genes.

A Factor Linking Floral Organ Identity and Growth Revealed by Characterization of the Tomato Mutant unfinished flower development (ufd)

“…In tomato, floral organ identity was partially or completely lost when representative genes of MADS-box classes A ( MC) , B ( SL, TM6, TPI and TPIB ), C ( TAG1 ), and E ( TM5 and TM29 ) were mutated or down-regulated (Lozano et al, 2009; Geuten and Irish, 2010; Quinet et al, 2014; Yuste-Lisbona et al, 2016), promoting homeotic changes in the floral organs where these gene functions are required. Additional floral whorls or floral organs were also observed in antisense TM5 plants and ectopic shoots with partially developed leaves and secondary flowers emerged from the fruit in antisense TM29 plants (Pnueli et al, 1994b; Ampomah-Dwamena et al, 2002). Furthermore, tomato mutations that altered regulatory genes involved in the activity and size of the FM as INFLORESCENCE MERISTEM ACTIVITY and the tomato homologous to CLAVATA genes have recently been isolated and further characterized (Sicard et al, 2008; Xu et al, 2015).…”

“…Sepals were suggested as the default state of floral organs and it was proposed that the activities of the FM identity genes during the specification of floral meristems could be involved in specifying sepal identity (Causier et al, 2010; Wellmer et al, 2014). It is true that the first whorl of tomato flowers seems to have a special status since mutations in MC only change sepal identity (Vrebalov et al, 2002; Yuste-Lisbona et al, 2016) while mutations of B- and C-class genes affect floral organs of two consecutive floral whorls and loss-of-function of E-class genes alter the three inner whorls (Pnueli et al, 1994b; Ampomah-Dwamena et al, 2002). In this context, UFD expression should be differently regulated in sepals and in the three innermost floral whorls.…”

“…The TOMATO AGAMOUS 1 ( TAG1 ) gene specifies stamen and carpel identity (Pnueli et al, 1994a) and together with TOMATO AGAMOUS LIKE-1 ( TAGL1 ; syn. ARLEQUIN ( ALQ ) (Vrebalov et al, 2009; Giménez et al, 2010), represent C-class gene function, while TM5 (Pnueli et al, 1994b) and TM29 (syn. TAGL2; Ampomah-Dwamena et al, 2002; Busi et al, 2003) have been proposed as E-class genes.…”

Genetic regulation and structural changes during tomato fruit development and ripening

“…Indeed, pistils are replaced by a reiteration of flowers in transgenic plants expressing TAG1 antisense (Pnueli et al, 1994) – just as in the Arabidopsis ag mutant (Yanofsky et al, 1990). In contrast, virtually complete silencing of TAG1 by RNAi does not affect pistil fate in this way instead, pistils develop into red fruits, indicating a loss of determinacy (Pan et al, 2010).…”

Functional Conservation and Divergence of Four Ginger AP1/AGL9 MADS–Box Genes Revealed by Analysis of Their Expression and Protein–Protein Interaction, and Ectopic Expression of AhFUL Gene in Arabidopsis

“…However, the ABC model is not sufficient to explain all angiosperm flowers; for example, Liliaceae flowers were exemplified by van Tunen et al [6] as the basis of a modified ABC model. The ABC model is still being modified to account for additional data from different plants [7] , particularly data on the formation of heterodimers or homodimers [8] – [11] , together with successive findings of E class and ovule–specific D class proteins in petunia, tomato, and Arabidopsis [12] – [16] . As a result, the classic ABC model was expanded to the “ABCDE model”, in which combinations of the A/B/C/D/E class genes specify the identity of each organ and control floral meristem determinacy [17] , [18] .…”