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      Baby don't cry, genetic regulation of the weeping phenotype in Prunus mume

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      Physiologia Plantarum
      Blackwell Publishing Ltd

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          Abstract

          Trees are an elegant and majestic lifeform and have for centuries been used by humans to create more pleasurable surroundings. One type of tree that perhaps sparks the imagination more than any other is one that exhibits the weeping branch phenotype. Recognized for their beauty, their drooping, downward facing branches makes them much sought after in parks and gardens. Despite a pretty clear idea of the structural difference of the weeping phenotype, little is known on the molecular regulation of the trait. In this issue of Physiologia Plantarum, Mao et al. ( 2020 ) screened for candidate genes related to the weeping phenotype to enhance our understanding of the molecular basis behind this characteristic way of growth. Though not typically found in nature, weeping trees have been cultivated for centuries for their elegance and adorn many a park and garden throughout the world. More than 500 weeping tree cultivars have been described of which some are grafted on the rootstock of a standard variety for support and others even need additional support without which they would grow as a weeping ground cover. This weeping trait is interesting from an architectural point of view but also deserves some attention from a biological point of view. In most cases stems grow upward, and during development obtain rigidity through secondary growth and the formation of tension wood on the upper side of the branch. This ultimately leads to structures strong enough to support their weight and defy gravity. In trees with the weeping trait the drooping branches have been attributed to alterations in wood formation such as faster elongation of cells than secondary (strengthening) growth, resulting in stems that lack the strength to support their weight and as a result start bending down (Hollender and Dardick 2015). Contrary to the physiology of weeping trees, much less is known on the genetics behind and the molecular regulation of this trait. In peach (Prunus persica) an allele was found, appropriately called WEEP, that at least partially is responsible for the trait (Hollender et al. 2018). In a totally different species, crape myrtle (Lagerstroemia), it was shown that genes involved in the biosynthesis and signaling of the plant hormone gibberellic acid (GA) play a major role in regulating the weeping phenotype (Li et al. 2020). GA has been hypothesized to play a role in the weeping phenotype in several species through its involvement in wood formation (reviewed by Hollender and Dardick 2015). In this issue of Physiologia Plantarum, Mao and colleagues take a close look at the weeping habit in Prunus mume, known commonly by several names including Mei, Japanese apricot and Japanese plum. By comparing differentially expressed genes and plant hormone levels between direct progeny of a weeping and an upright parent they aim to unravel part of the molecular network underlying the weeping trait (Fig. 1). What is interesting about their approach is that they take a detailed look at the lower (abaxial) and the upper (adaxial) side of a branch; as mentioned earlier, it is the tension wood on the adaxial side that contributes to a rigid and upright growing branch. The authors find a higher auxin (indole‐3‐acetic acid, IAA) content in the abaxial side of branches in upright progeny and a higher gibberellin (GA3) content in the adaxial side in weeping progeny with genes involved in the biosynthesis and signaling of these two hormones showing a similar pattern. The authors furthermore find two genes that encode key enzymes in lignin biosynthesis that where lower expressed in the weeping progeny. Less lignin production and a reduction in secondary growth via the interplay of IAA and GA3 might explain the lack of tensile strength in weeping branches in P. mume. Rather than focusing on finding a single causal gene, the authors have provided a comprehensive overview of transcriptional and hormonal changes in an effort to reveal the differences between ‘upright’ and ‘weeping’ plants. They show that it is a complex trait with several hormones and molecular processes involved. Though much work is still to be done in order to unravel the regulation of the weeping trait, this study provides an excellent and interesting step, helping us to understand why some trees cry.

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          Molecular basis of angiosperm tree architecture.

          The architecture of trees greatly impacts the productivity of orchards and forestry plantations. Amassing greater knowledge on the molecular genetics that underlie tree form can benefit these industries, as well as contribute to basic knowledge of plant developmental biology. This review describes the fundamental components of branch architecture, a prominent aspect of tree structure, as well as genetic and hormonal influences inferred from studies in model plant systems and from trees with non-standard architectures. The bulk of the molecular and genetic data described here is from studies of fruit trees and poplar, as these species have been the primary subjects of investigation in this field of science.
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            Loss of a highly conserved sterile alpha motif domain gene (WEEP) results in pendulous branch growth in peach trees

            Trees’ branches grow against the pull of gravity and toward light. Although gravity and light perception have been studied in model species, much is unknown about how trees detect and respond to these signals. Here, we report the identification of a gene ( WEEP ) that controls lateral branch orientations and is directly or indirectly required for gravity responses in trees. Loss or reduction of WEEP expression produced branches that grow outward and downward and did not exhibit normal gravitropism responses when displaced. WEEP is conserved throughout the plant kingdom and may be involved in gravity perception. WEEP may also be a valuable target for breeding or engineering trees with improved shapes for agricultural and landscaping applications. Plant shoots typically grow upward in opposition to the pull of gravity. However, exceptions exist throughout the plant kingdom. Most conspicuous are trees with weeping or pendulous branches. While such trees have long been cultivated and appreciated for their ornamental value, the molecular basis behind the weeping habit is not known. Here, we characterized a weeping tree phenotype in Prunus persica (peach) and identified the underlying genetic mutation using a genomic sequencing approach. Weeping peach tree shoots exhibited a downward elliptical growth pattern and did not exhibit an upward bending in response to 90° reorientation. The causative allele was found to be an uncharacterized gene, Ppa013325 , having a 1.8-Kb deletion spanning the 5′ end. This gene, dubbed WEEP , was predominantly expressed in phloem tissues and encodes a highly conserved 129-amino acid protein containing a sterile alpha motif (SAM) domain. Silencing WEEP in the related tree species Prunus domestica (plum) resulted in more outward, downward, and wandering shoot orientations compared to standard trees, supporting a role for WEEP in directing lateral shoot growth in trees. This previously unknown regulator of branch orientation, which may also be a regulator of gravity perception or response, provides insights into our understanding of how tree branches grow in opposition to gravity and could serve as a critical target for manipulating tree architecture for improved tree shape in agricultural and horticulture applications.
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              Transcriptome profiles reveal that gibberellin-related genes regulate weeping traits in crape myrtle

              Plant architecture includes vital traits that influence and benefit crops, and economically important trees. Different plant architectures provide natural beauty. Weeping ornamental plants are aesthetically appealing to people. The regulatory mechanism controlling the weeping trait is poorly understood in crape myrtle. To investigate the weeping trait mechanism, transcriptional profiling of different organs in weeping and upright crape myrtle was performed based on phenotype. Phenotypic and histological analyses demonstrated that endodermal cells were absent, and that new shoot phenotypes could be rescued by the GA3 treatment of weeping plants. The transcriptional analysis and coexpression network analysis (WGCNA) of differentially expressed genes indicated that GA synthesis and signal transduction pathways play a role in weeping traits. When the expression level of a negative element of GA signaling, LfiGRAS1, was reduced by virus-induced gene silencing (VIGS), new branches grew in infected plants in a negatively geotropic manner. An integrated analysis implied that GA had a strong influence on weeping crape myrtle by interacting with other factors. This study helps to elucidate the mechanism governing the weeping trait and can improve the efficiency of breeding in Lagerstroemia.
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                Author and article information

                Contributors
                sam.vanes@umu.se
                Journal
                Physiol Plant
                Physiol Plant
                10.1111/(ISSN)1399-3054
                PPL
                Physiologia Plantarum
                Blackwell Publishing Ltd (Oxford, UK )
                0031-9317
                1399-3054
                21 October 2020
                November 2020
                : 170
                : 3 ( doiID: 10.1111/ppl.v170.3 )
                : 315-317
                Affiliations
                [ 1 ] Department of Plant Physiology Umeå University Umeå Sweden
                Author information
                https://orcid.org/0000-0001-8042-3756
                Article
                PPL13229
                10.1111/ppl.13229
                7702079
                e22c9a61-1295-40ef-935c-6ed771b0bf9d
                © 2020 The Author. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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                Figures: 0, Tables: 0, Pages: 3, Words: 974
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                Custom metadata
                2.0
                November 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.4 mode:remove_FC converted:30.11.2020

                Plant science & Botany
                Plant science & Botany

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