Signaling network regulating plant branching: Recent advances and new challenges

doi:10.1016/j.plantsci.2021.110880

Plant Science

Volume 307, June 2021, 110880

https://doi.org/10.1016/j.plantsci.2021.110880 Get rights and content

Highlights

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We provide a critical overview on a current status of apical dominance (AD) research.
•
Presumed role for each hormone and sugar implicated in AD regulation was assigned.
•
New biochemical mechanisms of AD control involving mobile sugars are discussed.
•
Special role was suggested for positive feedback loops involving sugars and hormones.
•
Unresolved AD issues are highlighted, outlining the prospects for future studies.

Abstract

Auxin alone or supplemented with cytokinins and strigolactones were long considered as the main player(s) in the control of apical dominance (AD) and correlative inhibition of the lateral bud outgrowth, the processes that shape the plant phenotype. However, past decade data indicate a more sophisticated pathways of AD regulation, with the involvement of mobile carbohydrates which perform both signal and trophic functions. Here we provide a critical comprehensive overview of the current status of the AD problem. This includes insight into intimate mechanisms regulating directed auxin transport in axillary buds with participation of phytohormones and sugars. Also roles of auxin, cytokinin and sugars in the dormancy or sustained growth of the lateral meristems were assigned. This review not only provides the latest data on implicated phytohormone crosstalk and its relationship with the signaling of sugars and abscisic acid, new AD players, but also focuses on the emerging biochemical mechanisms, at first positive feedback loops involving both sugars and hormones, that ensure the sustained bud growth. Data show that sugars act in concert with cytokinins but antagonistically to strigolactone signaling. A complex bud growth regulating network is demonstrated and unresolved issues regarding the hormone–carbohydrate regulation of AD are highlighted.

Introduction

Emerging in the axils of the leaves of seed plants, the lateral buds after a short growth are usually inhibited in development and remain in a dormant state for some time, as long as they are not floral shoots of inflorescences [1]. The resumption of bud growth can be induced by removal of the terminal bud in the plant, leading to the assumption that the apical bud is an inhibitor of lateral buds. This phenomenon directly related to plant branching regulation is called apical dominance (AD). Despite its long-term study, this topic still remains at the center of attention of plant biologists. To date, a great body of experimental material has been accumulated on the mechanisms of the AD control of branching as well as genes involved in the regulation of dormancy/growth of lateral meristems. Studying the topic of AD and branching relies not only on academic interest, but may also be of practical importance for increasing plant productivity. For instance, the rice productivity increased by modulating activity of the gene IDEAL PLANT ARCHITECTURE 1 (IPA1)/SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 14 (SPL14) [[2], [3], [4], [5]] which takes part in the AD control [6,7]. The purpose of our paper is to provide an overview of the current status, unsolved problems and main prospects of the AD regulation research.

Currently, AD regulation appears as a network of interacting hormonal, trophic, and ontogenetic signals [8,9]. One of the first attempts to explain AD and correlative inhibition was initiated by botanists, followed by physiologists and they assumed that there is a competition of meristems for trophic resources, so-called trophic model [[10], [11], [12], [13]]. However, the question of how this proceeds remained long unanswered. Experiments on the replacement of the apical bud with lanolin paste with auxin, started more than 85 years ago, demonstrated the leading role of the apical auxin in inhibiting shoot branching [14]. To explain the auxin effect on the lateral meristem growth, two main mechanisms were suggested: auxin-transport model (AT-model) [[15], [16], [17]] and second messengers model (SM-model) [6,7,[18], [19], [20]], which were developed in parallel and in close interconnection. Paradoxically, the oldest trophic model was revived as well and acquired new content [8,[21], [22], [23]]. The phytochrome regulation of AD is not considered here, since this issue was covered in sufficient details in a recent review [9] as well as in [[24], [25], [26], [27], [28], [29]], stressing the inhibitory role of abscisic acid (ABA) in axillary bud growth.

Section snippets

Second messengers of auxin in AD regulation

Auxin indole-3-acetic acid (IAA) is synthesized in young apical leaves [30,31] and polarly transported down the stem due to membrane-located carrier proteins [32]. The key IAA biosynthesis enzymes are TRYPTOPHAN AMINOTRANSFERASE related proteins (TAR) which convert tryptophan to indole-3-pyruvic acid (IPyA) [[33], [34], [35]], and YUCCA flavin monooxygenase-like enzymes which convert IPyA to IAA. Overexpression of YUC genes leads to auxin overproduction [36,37]. The polar/asymmetric subcellular

A role of auxin integral status in bud behavior

Synthesis of IAA and its polar transport are the basis for growth, organogenesis and histogenesis in the development of shoot apical meristem and the entire plant body [30,31,146,147]. The integrated action of auxin synthesis, transport and metabolism defines the spatiotemporal pattern of auxin accumulation [31]. This IAA accumulation in defined sites induces their organogenesis and the formation of new leaf primordia, determining loci of meristemic growth and layers of procambium in young

Sugars, as an auxin-independent signal controlled by sink-source relationship, play an important role in AD regulation

The detection of an auxin-independent AD signal was first noted by Prasad and Cline [186] who have found that gibberellin-induced growth of the main shoot inhibited the outgrowth of axillary buds in inverted Pharbitis nil plants. Thus, the classical theory of apical dominance: assimilate diversion and uptake by the intensively growing apex, has received a support as a mechanism for maintaining axillary buds in a dormant state due to nutrient deficiency. More recently, Tarancón et al. [187]

Concluding remarks

Here we aim to recapitulate the advances of the world long-term study of AD regulation, by proposing the model for bud behavior. To date, a significant progress has been achieved in understanding the regulation of axillary bud growth by hormones (auxins, CKs and SLs) and sugars as signaling molecules. It is now commonly accepted that axillary bud outgrowth is regulated by a complex hormonal/metabolic network. Sugars, the activators of the bud growth and which allocation governs the sink-source

Funding

This work was supported by the Ministry of Science and Higher Education of the Russian Federation (No АААА-А19-119041690035-9).

Declaration of Competing Interest

None.

Acknowledgements

We thank Dr. Elena Sheveleva for her assistance in English correction.

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Review articleSignaling network regulating plant branching: Recent advances and new challenges

Highlights

Abstract

Introduction

Section snippets

Second messengers of auxin in AD regulation

A role of auxin integral status in bud behavior

Sugars, as an auxin-independent signal controlled by sink-source relationship, play an important role in AD regulation

Concluding remarks

Funding

Declaration of Competing Interest

Acknowledgements

Mol. Plant

Trends Plant Sci.

Trends Plant Sci.

Trends Genet.

Eur. J. Cell Biol.

Cell

Curr. Opin. Plant Biol.

J. Plant Physiol.

Curr. Opin. Plant Biol.

J. Biol. Chem.

Trends Plant Sci.

Curr. Biol.

Anatomy of Seed Plants

Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice

Nat. Genet.

Tissue-specific ubiquitination by IPA1 INTERACTING PROTEIN 1 modulates IPA1 protein levels to regulate plant architecture in rice

Plant Cell

Strigolactone inhibition of shoot branching

Nature

Inhibition of shoot branching by new terpenoid plant hormones

Nature

Light regulation of axillary bud outgrowth along plant axes: an overview of the roles of sugars and hormones

Front. Plant Sci.

Chemical basis of correlation I. Production of equal masses of shoots by equal masses of sister leaves in Bryophyllum calycinum

Bot. Gaz.

Regeneration from a Physico-chemical Viewpoint

The correlative inhibition of the growth of axillary buds

Ann. Bot.

The young leaf as the inhibiting organ

New Phytol.

Studies on the growth hormone of plants III: the inhibitory action of the growth substance on bud development

Proc. Natl. Acad. Sci. U. S. A.

Cytokinin targets auxin transport to promote shoot branching

Plant Physiol.

Connective auxin transport contributes to strigolactone-mediated shoot branching control independent of the transcription factor BRC1

PLoS Genet.

Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance

Plant J.

The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching

Plant Physiol.

Antagonistic action of strigolactone and cytokinin in bud outgrowth control

Plant Physiol.

Sugar demand, not auxin, is the initial regulator of apical dominance

Proc. Natl. Acad. Sci. U. S. A.

Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida

J. Exp. Bot.

Sugar suppresses the auxin-induced strigolactone pathway to promote bud outgrowth

New Phytol.

Abscisic acid regulates axillary bud outgrowth responses to the ratio of red to far-red light

Plant Physiol.

BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis

Plant Cell

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

Proc. Natl. Acad. Sci. U. S. A.

Identification of gene functions associated to active and dormant buds in Arabidopsis

Plant Signal. Behav.

Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth

Plant Physiol.

The ratio of red light to far red light alters Arabidopsis axillary bud growth and abscisic acid signalling before stem auxin changes

J. Exp. Bot.

Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth

Plant J.

Auxin at the shoot apical meristem

Cold Spring Harb. Perspect. Biol.

A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis

Plant Cell

The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis

Plant Cell

Review article
Signaling network regulating plant branching: Recent advances and new challenges