Plant developmental oddities

Abstract

Plants lacking shoot apical meristem develop with unique body shapes, suggesting rewiring of developmental genes. This loss of the meristem is likely influenced by a combination of environmental factors and evolutionary pressures. This study explores the development of plant bodies in three families (Podostemaceae, Lemnaceae, and Gesneriaceae) where the shoot apical meristem (SAM), a key structure for growth, is absent or altered. The review highlights alternative developmental strategies these plants employ. Also, we considered alternative reproduction in those species, namely through structures like turions, fronds, or modified leaves, bypassing the need for a SAM. Further, we report on studies based on the expression patterns of genes known to be involved in SAM formation and function. Interestingly, these genes are still present but expressed in atypical locations, suggesting a rewiring of developmental networks. Our view on the current literature and knowledge indicates that the loss or reduction of the SAM is driven by a combination of environmental pressures and evolutionary constraints, leading to these unique morphologies. Further research, also building on Next-Generation Sequencing, will be instrumental to explore the genetic basis for these adaptations and how environmental factors influence them.

Keywords: Bauplan; Evolutionary adaptation; Phytomer; Plant development; SAM.

Fig. 1

a Conceptual model, for a generic dicot species, of a late-heart embryo. b Vegetative shoot apical meristem of a model dicot species that has just initiated a leaf primordium as a consequence of the interplay of STM, WUS, CLV3, ARP, and CUC. WUS is transcribed in the OC and activates CLV3/CLV1, that in turn inhibits WUS. STM is expressed in the SAM and is repressed by ARP in the leaf primordium. CUC marks the boundary between leaf primordium and AM. The layers L1–L3 are indicated by dome-shaped lines. Color code: green dots (a) and vivid green area (b): CUC; red dots (a) and area delimited by red hatched line (b): STM; yellow area (a) and yellow dots (b): CLV. In this context, CLV refers to the area where both CLV3 and CLV1 are present; blue dots: WUS

Fig. 2

Unorthodox plant morphology of Lemnaceae, Gesneriaceae, and Podostemaceae. a Aerial view of the body of the Landoltia (Lemnaceae), where the dormant vegetative buds (turions) are represented; b Lemna (Lemnaceae): mother frond with two budding pouches; D1, daughter frond and D2, smaller daughter frond. Note that these tissues are partially covered by the MF; c Streptocarpus (Gesneriaceae): rosulate plant with cotyledonary phyllomorph (Ph); P1-P3 additional phyllomorphs formed in numbered succession; d Hydrobryum (Podostemaceae): Ribbon like branching roots (R) with adventitious tufts of leaves on flank (L). T turion, aerial view, MF mother frond, DF daughter frond, arising from the budding pouch, R root, L leaf. Bar: 1 mm in a and b, 1 cm in c, and 3 mm in d

Fig. 3

Comparative schematic representation of the early body plan of different plants. a A. thaliana; b Tristichoideae; c Weddellinoideae; d Podostemoideae (Zeylanidium); e Podostemoideae (Hydrobryum). co cotyledon, R root; AR adventitious root, AS adventitious shoot, L leaf-like structure, Rh rhizoid, H hypocotyl, RAM and SAM red circle. The partially functional pseudo-SAM of Zeylanidium is represented by a red crescent. The AS is indeterminate in c and determinate in d and e (lacking SAM)

Fig. 4

Schematic representation of gene expression in the root of Hydrobryum japonicum. a WUS (blue dots) and STM (red dots) are expressed in the root at the site of formation of the first leaf primordium; b STM and WUS are expressed during the initiation and formation of a leaf; c A new leaf primordium arises at the base of the previous one, where both WUS and STM are expressed. L1 youngest leaf, L2 leaf following L1, L3 oldest leaf. Red dots: STM; blue dots: WUS; green dots: ARP; dashed line: abscission-like vacuolated cells

Fig. 5

Schematic illustration of gene expression pattern during the early development of Zeylanidium tailychenoides. a CUC3 expression (green) at the base of the cotyledon at the onset of a new shoot-like structure; b STM expression (red) at the site where the new shoot develops (S1); CUC3 expression (green) where the next shoot primordium (S2) is originating; c STM (red) expression at S1 and S2. co cotyledon, Rh rhizoid. The inset provides the details of the pattern of gene expression

Fig. 6

Schematic representation of the formation of micro- (mc) and macrocotyledons (Mc) in Streptocarpus rexii. a Isocotiledonary early stage; b Anisocotyledonary stage; c formation of the first phyllomorph. The figure also reports the gene expression patterns in seedlings of Streptocarpus rexii. a The orthologs of STM and WUS are expressed in both cotyledons during early stage of germination; b STM, WUS, and ARP transcripts are present in the basal meristem (Bm) of the macrocotyledon (Mc); c later stage of development, where STM, WUS, and ARP are expressed in the Bm of the phyllomorph (Ph) and in the groove meristem (Gm). Bm basal meristem, Pm petiolode meristem, Gm groove meristem, co microcotyledon. Color code: red dots, STM expression; blue dots, WUS; green dots, ARP; blue area: Bm; light red area: Gm; yellow area: Pm. The insets provide details of the pattern of genes expression

Fig. 7

Schematic representation of the morphological differences between the three families considered, and the manifestation of SAM-like growth. Dark green sphere: SAM; small green spheres: regions of displacement of the meristematic activity