JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development.

Abscission is a universal and dynamic process in plants whereby organs such as leaves, flowers and fruit are shed, both during normal development, and in response to tissue damage and stress. Shedding occurs by separation of cells in anatomically distinct regions of the plant, called abscission zones (AZs). During abscission, the plant hormone ethylene stimulates cells to produce enzymes that degrade the middle lamella between cells in the AZ. The physiology and regulation of abscission at fully developed AZs is well known, but the molecular biology underlying their development is not. Here we report the first isolation of a gene directly involved in the development of a functional plant AZ. Tomato plants with the jointless mutation fail to develop AZs on their pedicels and so abscission of flowers or fruit does not occur normally. We identify JOINTLESS as a new MADS-box gene in a distinct phylogenetic clade separate from those functioning in floral organs. We propose that a deletion in JOINTLESS accounts for the failure of activation of pedicel AZ development in jointless tomato plants.

Interactions between jointless and wild-type tomato tissues during development of the pedicel abscission zone and the inflorescence meristem.

The jointless mutation of tomato results in the formation of flower pedicels that lack an abscission zone and inflorescence meristems that revert to vegetative growth. We have analyzed periclinal chimeras and mericlinal sectors of jointless and wild-type tissue to determine how cells in different meristem layers (L1, L2, and L3) and their derivatives interact during these two developmental processes. Cells in the inner meristem layer, L3, alone determined whether the meristem maintained the inflorescence state or reverted to vegetative growth. Moreover, L3 derivatives determined whether a functional pedicel abscission zone formed. Limited and disorganized autonomous development of wild-type L2-derived cells occurred when they overlay mutant tissue. Adjacent mutant and wild-type L3-derived tissues in pedicels developed autonomously, indicating little or no lateral communication. Only the outermost L3-derived cells within the pedicel were capable of orchestrating normal pedicel development in overlying tissues, revealing the special status of those cells as coordinators of development for L1- and L2-derived cells, whereas the innermost L3-derived cells developed autonomously but did not influence the development of other cells.

Effect of lateral suppressor on petal initiation in tomato.

Flowers developing on tomato (Lycopersicon esculentum) plants homozygous for the lateral suppressor (ls) mutation lack petals. Scanning electron micrographs revealed that in ls plants no second whorl organs were initiated. The initiation of first, third, and fourth whorl organs were unaffected by this mutation. To investigate interactions between the cells in different layers of the floral meristem during organ initiation, a periclinal chimera between wild-type and ls tomato was generated. Flowers of the chimera having ls cells in the outer meristem layer (L1) and wild-type cells in internal layers (L2 and L3) developed normally, including the initiation of organ primordia that differentiated as petals in normal positions within the second whorl. L1 of the chimera developed in a non-autonomous manner during petal development. Thus, wild-type cells occupying the internal meristem layers provided developmental cues necessary for initiation of petal primordia at appropriate positions on the floral meristem. L1 cells carrying the lateral suppressor mutation were fully capable of responding to this information and differentiated appropriately.

The internal meristem layer (L3) determines floral meristem size and carpel number in tomato periclinal chimeras.

Cell-cell interactions are important during plant development. We have generated periclinal chimeras between plants that differ in the number of carpels per flower to determine the roles of cells occupying specific positions in the floral meristem in determining the number of carpels initiated. Intraspecific chimeras were generated between tomato (Lycopersicon esculentum) expressing the mutation fasciated, which causes an increased number of floral organs per whorl, and tomato wild type for fasciated. Interspecific chimeras were generated between tomato and L. peruvianum, which differ in number of carpels per flower. In both sets of chimeras, carpel number as well as the size of the floral meristem during carpel initiation were not determined by the genotype of cells in the outer two layers of the meristem (L1 and L2) but were determined by the genotype of cells occupying the inner layer (L3) of the meristem. We concluded from these experiments that during floral organ initiation, cells in certain layers of the meristem respond to information supplied to them from other cells in the meristem.

Chimeric tomato plants show that aphid resistance and triacylglucose production are epidermal autonomous characters.

Graft chimeras were generated using Lycopersicon pennellii and L. esculentum to determine the contribution of the three meristem layers (L1, L2, and L3) to trichome density, sugar ester production, and aphid resistance. Sugar esters, in the form of triacylglucoses, have been implicated in the aphid resistance of pennellii. One chimera possessed the epidermal layer (L1) of pennellii and the internal tissues (L2 and L3) of the aphid-susceptible esculentum. The second chimera had both the L1 and L2 of pennellii and the L3 of esculentum. Type IV trichome densities did not differ significantly among the chimeras and pennellii. Both chimeras accumulated sugar esters with similar sugar and fatty acid composition as pennellii. The concentration of epicuticular sugar ester on the chimeras was also comparable with that of pennellii. Leaf cage and feeding studies demonstrated that both chimeras are as resistant to aphids as is pennellii. The resistance could be reduced similarly on all three types of plants by removal of the type IV trichome exudate. These results indicate that the presence and density of the type IV trichomes and the amount and type of sugar esters produced are features determined by the genotype of the epidermis. These epidermal features are sufficient to account for the aphid resistance observed in pennellii.