Strategy for shoot meristem proliferation in plants

Abstract

Shoot apical meristem (SAM) of plants harbors stem cells capable of generating the aerial tissues including reproductive organs. Therefore, it is very important for plants to control SAM proliferation and its density as a survival strategy. The SAM is regulated by the dynamics of a specific gene network, such as the WUS-CLV interaction of A. thaliana. By using a mathematical model, we previously proposed six possible SAM patterns in terms of the manner and frequency of stem cell proliferation. Two of these SAM patterns are predicted to generate either dichotomous or axillary shoot branch. Dichotomous shoot branches caused by this mechanism are characteristic of the earliest vascular plants, such as Cooksonia and Rhynia, but are observed in only a small minority of plant species of the present day. On the other hand, axillary branches are observed in the majority of plant species and are induced by a different dynamics of the feedback regulation between auxin and the asymmetric distribution of PIN auxin efflux carriers. During evolution, some plants may have adopted this auxin-PIN system to more strictly control SAM proliferation.

SAM Pattern is Limited by Developmental Constraints

Shoot apical meristem (SAM) of plants is located at the tip of the shoot and has stem cells that generate the aerial parts including reproductive organs. Thus, it is very important for plants to control SAM proliferation and keep an appropriate density of the SAM as a survival strategy. Presumably, the fitness function would have its maximum at an optimum density of the SAM, while the density higher or lower than this optimum would reduce the fitness (Fig. 1). Therefore, plants will evolve their SAM density toward the optimum. On the other hand, the SAM proliferation is limited by developmental constraints. The SAM development is regulated by the dynamics of a specific gene network, such as the WUSCEL (WUS)-CLAVATA (CLV) interaction of A. thaliana.^1,2 We recently proposed a mathematical model based on this molecular dynamics and provided a theoretical explanation for various SAM patterns observed in plants.³ In our model, SAM pattern is determined by two factors: mode of stem cell proliferation and stem cell containment (Fig. 2). The modes of stem cell proliferation can be classified into four groups based on regulatory strengths in the WUS-CLV dynamics: elongation mode, division mode, emergence mode, and fluctuation mode (Fig. 2).³ On the other hand, the stem cell containment is associated with the spatial restriction of the WUS-CLV gene network dynamics. The combination of these two factors predicts six possible SAM patterns in terms of the manner and speed of stem cell proliferation (Fig. 2).

Figure 1.

Fitness function of SAM density. The fitness has a maximum at an optimum density of the SAM, and decreases in larger and smaller densities.

Figure 2.

SAM patterns predicted by the model. SAM patterns are classified into six groups that are determined by the combination of the mode of stem cell proliferation and stem cell containment. The elongation mode and the fluctuation mode give rise to fasciation pattern (clv mutant of A. thaliana) and fluctuation pattern (wus), respectively. In the division mode and the emergence mode, SAM pattern is largely affected by the stem cell containment. While the weak containment condition produces the multiplication pattern (amp1/pt and uni-1D), the strong containment results in the homeostasis pattern (pin1). On the other hand, under the intermediate condition, the division mode and the emergence mode generate dichotomous pattern and monopodial pattern, respectively, both of which are associated with shoot branching. The dichotomous pattern is found in clv of A. thaliana and klavier of L. japonicus, but there is no evidence that the monopodial pattern is present in plants. Blue spots indicates the stem cell activity.

Although our model is originally based on experimental results in A. thaliana, the outcome of the model is applicable to all plant species because it is not influenced by variations in the regulatory structure of the gene network dynamics controlling the SAM. Therefore, any given SAM morphology in plants can be explained by one of the six patterns predicted by the model. In this article, we will briefly discuss the SAM proliferation patterns, more specifically, SAM patterns associated with shoot branching.

Plant Strategy for SAM Proliferation

The activity of the stem cell reflects that of the SAM-specific genes, such as WUS and CLV3 of A. thaliana.^1,2 These genes are strongly expressed in a single spot at the meristem center of wild-type plants. However, the fluctuation mode in our model is predicted to generate aberrant stem cell patterns of multiple spots with very weak expression of such SAM-specific genes, while the elongation mode likely produces elongated structures (Fig. 2).³ Therefore, these proliferation modes possibly reduce the fertility and, hence, the fitness of plants. Indeed, the A. thaliana wus mutant (an example of the fluctuation mode) is completely sterile.⁴ In addition, clv mutants (an example of the elongation mode) produce deformed siliques, resulting in reduced fertility.^5-10

On the other hand, both the division mode and the emergence mode can give rise to stem cell spots with strong expressions of the SAM-specific genes, and are thus expected to form functional SAMs. In these two modes, shoot morphology is determined by the frequency of SAM multiplication that depends on the strength of the stem cell containment (Fig. 2). The weak containment causes the multiplication pattern that shows a runaway proliferation of the SAM, leading to formation of many adventitious buds (Fig. 2). This morphological feature is observed in amp1/pt and uni-1D of A. thaliana.^11,12 In contrast, the SAM never multiplies under the strong containment condition, resulting in the homeostasis pattern in which only a main shoot axis elongates without branches (Fig. 3A). The intermediate containment causes the dichotomous and monopodial patterns, in which the SAM gradually multiplies one by one and then the daughter SAMs independently produce shoot branches (Fig. 3BC). Therefore, it is possible that the dichotomous and monopodial patterns are the most adaptive strategies for SAM proliferation among the six possible patterns predicted by our model.

Figure 3.

Shoot branching caused by the SAM multiplication. The SAM is maintained by a specific gene regulatory network for the SAM maintenance, such as the WUS-CLV dynamics of A. thaliana. This molecular dynamics can generate a shoot axis with no branches in the homeostasis pattern (A), a dichotomous branch in the dichotomous pattern (B), or an axillary branch in the monopodial pattern (C). However, these shoot patterns are observed in only a small minority of vascular plant species of the present day. (D) On the other hand, the majority of plant species shows axillary branches that are induced by the auxin-PIN dynamics. In this case, an auxin maximum is initially formed at a point distant from the pre-existing stem cells, and then activates the WUS-CLV dynamics, resulting in formation of an axillary shoot. Blue and magenta spots indicate stem cells that are multiplied by the WUS-CLV dynamics and the ones that are induced by the auxin-PIN system, respectively. Orange spot indicates an auxin maximum.

(1) Dichotomous branching by the dichotomous pattern

In the dichotomous pattern, a shoot will elongate with iterated dichotomous branching, in which a SAM is laterally elongated and then divided equally into two daughter meristems (Figs. 3B and4). This morphological feature is characteristic of the earliest known vascular plants, such as Cooksonia and Rhynia, which are considered to be ancestral to present-day plants.¹³ In addition, this branching pattern is observed in a small minority of plant species of today, such as whisk fern (Psilotum nudum) and mistletoe (Viscum album), and is also reported in morphological mutants, including clv of A. thaliana^14,15 and klavier^16,17 or LjCLV3-silenced lines¹⁸ of L. japonicus.

Figure 4.

Schematic diagram of morphological transition of plant shoots. The homeostasis pattern produces a main shoot axis with no branches, which is exemplified by pin1 of A. thaliana. The dichotomous pattern, monopodial pattern, and fasciation pattern can generate dichotomous shoot branches, axillary shoot branches, and fasciated shoots, respectively. However, these shoot patterns are observed only in the minority of plant species of the present day. On the other hand, the majority of vascular plant species shows axillary branches that are induced by another dynamics of the auxin-PIN system. Blue and magenta spots indicate SAMs that are generated by the WUS-CLV dynamics and the ones that are induced by the auxin-PIN system, respectively.

(2) Axillary branching by the monopodial pattern

In the monopodial pattern, a shoot will elongate with iterated axillary branching, in which a new SAM emerges at a point distant from the pre-existing one (Figs. 3C and4). However, there is no definitive evidence so far that this dynamics is actually responsible for axillary shoot branches of plants. Because the monopodial pattern in the model occurs only in a very restricted parameter space, there is a very small possibility that this pattern exists in plants.³

(3) Axillary branching induced by the auxin-PIN dynamics

Our previous numerical simulations demonstrated that the dichotomous and monopodial patterns can form shoot branches, but have large fluctuations in the period of branch generation.³ This finding suggests that plants cannot strictly control SAM proliferation using these mechanisms alone. Thus, plants may have evolved another specific system for SAM multiplication to more strictly control the meristem density. In fact, axillary branches observed in many vascular plant species are probably induced by the auxin-PIN system (Fig. 3D and4), because plants defective in this dynamics show a typical homeostasis pattern in which an inflorescence shoot elongates without branches.¹⁹

(4) Fasciation

The fasciation pattern produces an elongated SAM and the resulting flattened stem (Fig. 4). This morphological abnormality is well known as fasciation, which is observed in various plant species in a natural environment as well as under laboratory conditions.²⁰ In addition, fasciated shoots are also found in several garden varieties, such as Japanese fantail willow (Salix sachalinensis) and feather cockscomb (Celosia cristata).²⁰

Concluding Remarks

The SAM of plants is maintained by a specific gene regulatory network, such as the WUS-CLV dynamics of A. thaliana. This molecular dynamics can generate both dichotomous and axillary shoot branches by multiplying the SAM. The dichotomous branching by this mechanism is characteristic of the earliest known vascular plants, but is observed only in a small minority of plant species of the present day. On the other hand, the majority of plant species has axillary branches that are induced by the distinct dynamics of auxin and PIN auxin efflux carriers. Plants may have evolved the functional differentiation between the maintenance and multiplication of the SAM. The auxin-PIN system may have been adopted for the latter purpose, allowing for more strict control of the SAM proliferation.

Glossary

Abbreviations:

SAM

shoot apical meristem

WUS

WUSCHEL

CLV

CLAVATA

Fujita H, Toyokura K, Okada K, Kawaguchi M. Reaction-diffusion pattern in shoot apical meristem of plants. PLoS One. 2011;6:e18243. doi: 10.1371/journal.pone.0018243.