From thin to thick: major transitions during stem development

Abstract

The variability of shoot architecture in plants is striking and one of the most extreme examples of adaptive growth in higher organisms. Mediated by the differential activity of apical and lateral meristems, flexibility in stem growth essentially contributes to this variability. In spite of this importance, the regulation of major events in stem development is largely unexplored. Recently, however, novel approaches exploiting knowledge from root and leaf development are starting to shed light on molecular mechanisms that regulate this essential plant organ. In this review, we summarize our understanding of initial patterning events in stems, discuss prerequisites for the initiation of lateral stem growth and highlight the burning questions in this context.

Figure 1

(a) Schematic representation of the phytomer concept proposed for plant shoots. Phytomers along the shoot are sequentially labeled from young to old and include one leaf (L), one axillary bud (AB) and one associated stem fragment each. SAM, Shoot apical meristem. (b, c) Comparison of cross-sections from a primary (b) and secondary (c)Arabidopsis stem. Pictures taken and adapted from .

Figure 2

Schematic representation of typical tissue patterns in different organs of vascular plants. (a) Typical stages and organization of a shoot of a dicotyledonous plant. After establishment of the primary pattern, a tube-like domain of meristematic activity is established that transforms the primary into a secondary stem. (b) The protostele contains a central and concentric vascular system. It is regarded as being the most ancient tissue organization in vascular plant stems and is found in juvenile plants of many extant ferns. (c) General organization of a typical leaf. (d) Actinostele as usually found in roots of vascular plants. (e) The eustele is typical for stems of Magnoliids and Eudicotyledons and is characterized by a parenchymatous pith in the stem center and collateral bundles. Individual bundles are separated to various degrees by parenchymatous rays. (f) The atactostele as usually found in stems of monocotyledons. A common endodermis encompassing the whole stele is sometimes present. (g) In stems of rev-10d gain-of-function and in phv phb cna or kan1,2,3 triple mutants, vascular bundles are radialized and shifted towards the stem center. (h)shr and scr mutants fail to establish a starch sheath. (i) Differentiation of peripheral tissues is disturbed in bp/knat1 mutants. Abbreviations: CZ, central zone; IC, interfascicular cambium; Px, leaf primordial; PZ, peripheral zone; RZ, rib zone; SAM, shoot apical meristem; VB, vascular bundle.

Figure 3

Analysis of various gene expression patterns in different Arabidopsis organs. (a)ATHB8 transcript accumulation in procambial strands (arrowheads) as visualized by RNA in situ hybridization indicates the early initiation of vascular tissue in lateral organs. A longitudinal section through a generative apex is shown. The asterisk denotes the SAM. (b) As indicated by the activity of a STM:GUS reporter , the STM promoter is active in differentiated tissues of vascular bundles in stems. (c) The SCR:GFP marker visualizes the starch sheath at the bottom of stems of 15-cm-tall plants (green signal). The rough hand section was counterstained with propidium iodide (red signal). Asterisks label the position of primary vascular bundles. (d, e) RNA in situ hybridizations of vegetative shoot apices reveal an early activation of WOX4 (d) in vascular bundles of leaf primordia which is, however, later than the activation of the ‘preprocambial’ marker ATHB8(e). Arrows indicate the youngest primordia in which respective transcript accumulation is detectable. Asterisks label the SAM. Scale bars: 100 μm. Same magnification in (d) and (e). RNA in situ hybridizations were performed as described previously . Abbreviations: FC, Fascicular cambium; FP, flower primordium; IF, interfascicular fibers; Ph, phloem; SS, starch sheath; Xy, xylem.