Chiral events in developing gametophores of Physcomitrella patens and other moss species are driven by an unknown, universal direction‐sensing mechanism

Abstract

Premise of the Study We used the model species Physcomitrella patens to examine chirality in moss gametophores. Chirality is manifested in the direction of consecutive apical cell divisions, cell plate configurations, and deviations of leaf connecting lines from the vertical course. However, the frequencies of chiral configurations of all these processes as well as their mutual dependence—especially in the case of gametophore branching—are not known. Other moss species were checked to determine the universality of our findings. Methods The gametophore structure of Physcomitrella patens grown in the laboratory under controlled conditions was investigated using light microscopy and compared with that of other moss species collected from their natural stands. Key Results In all investigated moss species, the tetrahedral apical cell exhibits either clockwise or counterclockwise consecutive divisions, and selection of this directionality in the primary axis is random. It is, however, related to cell plate configuration. If the plate is skewed, leaf‐producing segments arising from the apical cell cleavage exhibit circumferential rotation. Three parallel lines connecting the leaves deviate from a vertical course, but always in the same direction as that of leaf initiation; thus, the angular distance between consecutive leaves increases to >120°. Lateral branches are exclusively antidromous. Conclusions Gametophore chiral configuration appears to be useful in resolving problems of moss modular growth and branching. Morphological and anatomical evidence strongly suggests that an unknown direction‐sensing mechanism controls the development of moss axial organs. We propose that leaves are responsible for a horizontal gradient of sugar signals that develops along the gametophore circumference, thus influencing branching‐unit chirality.

Mirror Symmetry of Life

“…Their tetrahedral AC, watched from its triangular base, divides either CW or CCW and this direction is randomly established in the development of the gametophore main axis. However, it is not so in the case of its lateral branches -the chirality of their AC is always opposite to that of the supporting axis [5]. It is possible that this antidromic correlation triggers the horizontal gradient of some putative signals vertically transported from the neighboring leaves of gametophore (Figure 5).…”

“…Not only structures but also some developmental processes may be chiral. The apical cell divisions in moss gametophores [5], cell cleavage in the embryos of snails [6,7] or lateral organ initiation on plant shoot apical meristem (SAM) proceed clockwise (CW) or counterclockwise (CCW). Two interesting problems may be addressed while considering chiral structures in biological systems -mechanism of their formation and proportion between the two chiral configurations.…”

Phyllotaxis from a Single Apical Cell

“…Each asymmetric cleavage of the apical cell produces a leaf initial and perpetuates the apical cell itself to sustain shoot growth, as evidenced by live imaging of physcomitrium shoot buds [9]. The relationship between apical cell division angle and resulting phyllotactic patterns has mainly been inferred from histological observations of fixed specimens [6,13,14]. In some moss species, the apical cell is lenticular with two alternating division planes that produce opposite segments (j = 1, a = 180°), resulting in distichous phyllotaxis like in Fissidens (Figure 1A, 1B).…”

Verbena officinalis Verbenaceae (Lamiales): a new plant model system for phyllotaxis research

“…The regular distribution of lateral organs in plant axial systems, called phyllotaxis, has intrigued scientists for a long time. Interesting examples of this universal phenomenon have been found among brown algae (Peaucelle and Couder 2016 ), leafy bryophytes (Zagórska-Marek et al 2018 ), clubmosses (Gola 1996 ; Yin and Meicenheimer 2016 ), and seed plants (Yin et al 2011 ; Zagórska-Marek 1985 ; for review see Gola and Banasiak 2016 ). The best known and most common are whorled or spiral phyllotactic patterns, and among the latter, the main Fibonacci pattern prevails.…”