TY  - JOUR
A1  - Sicard, Adrien
A1  - Kappel, Christian
A1  - Lee, Young Wha
A1  - Wozniak, Natalia Joanna
A1  - Marona, Cindy
A1  - Stinchcombe, John R.
A1  - Wright, Stephen I.
A1  - Lenhard, Michael
T1  - Standing genetic variation in a tissue-specific enhancer underlies
selfing-syndrome evolution in Capsella
JF  - Proceedings of the National Academy of Sciences of the United States of America
N2  - Mating system shifts recurrently drive specific changes in organ dimensions. The shift in mating system from out-breeding to selfing is one of the most frequent evolutionary transitions in flowering plants and is often associated with an organ-specific reduction in flower size. However, the evolutionary paths along which polygenic traits, such as size, evolve are poorly understood. In particular, it is unclear how natural selection can specifically modulate the size of one organ despite the pleiotropic action of most known growth regulators. Here, we demonstrate that allelic variation in the intron of a general growth regulator contributed to the specific reduction of petal size after the transition to selfing in the genus Capsella. Variation within this intron affects an organ-specific enhancer that regulates the level of STERILE APETALA (SAP) protein in the developing petals. The resulting decrease in SAP activity leads to a shortening of the cell proliferation period and reduced number of petal cells. The absence of private polymorphisms at the causal region in the selfing species suggests that the small-petal allele was captured from standing genetic variation in the ancestral out-crossing population. Petal-size variation in the current out-crossing population indicates that several small-effect mutations have contributed to reduce petal-size. These data demonstrate how tissue-specific regulatory elements in pleiotropic genes contribute to organ-specific evolution. In addition, they provide a plausible evolutionary explanation for the rapid evolution of flower size after the out-breeding-to-selfing transition based on additive effects of segregating alleles.
KW  - morphological evolution
KW  - growth control
KW  - standing variation;
 organ-specific evolution
KW  - intronic cis-regulatory element
Y1  - 2016
U6  - https://doi.org/10.1073/pnas.1613394113
SN  - 0027-8424
VL  - 113
SP  - 13911
EP  - 13916
PB  - National Acad. of Sciences
CY  - Washington
ER  - 
TY  - JOUR
A1  - Huu, Cuong Nguyen
A1  - Keller, Barbara
A1  - Conti, Elena
A1  - Kappel, Christian
A1  - Lenhard, Michael
T1  - Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene
JF  - Proceedings of the National Academy of Sciences of the United States of America (PNAS)
N2  - Heterostyly represents a fascinating adaptation to promote outbreeding in plants that evolved multiple times independently. While L-morph individuals form flowers with long styles, short anthers, and small pollen grains, S-morph individuals have flowers with short styles, long anthers, and large pollen grains. The difference between the morphs is controlled by an S-locus "supergene" consisting of several distinct genes that determine different traits of the syndrome and are held together, because recombination between them is suppressed. In Primula, the S locus is a roughly 300-kb hemizygous region containing five predicted genes. However, with one exception, their roles remain unclear, as does the evolutionary buildup of the S locus. Here we demonstrate that the MADS-box GLOBOSA2 (GLO2) gene at the S locus determines anther position. In Primula forbesii S-morph plants, GLO2 promotes growth by cell expansion in the fused tube of petals and stamen filaments beneath the anther insertion point; by contrast, neither pollen size nor male incompatibility is affected by GLO2 activity. The paralogue GLO1, from which GLO2 arose by duplication, has maintained the ancestral B-class function in specifying petal and stamen identity, indicating that GLO2 underwent neofunctionalization, likely at the level of the encoded protein. Genetic mapping and phylogenetic analysis indicate that the duplications giving rise to the style-length-determining gene CYP734A50 and to GLO2 occurred sequentially, with the CYP734A50 duplication likely the first. Together these results provide the most detailed insight into the assembly of a plant supergene yet and have important implications for the evolution of heterostyly.
KW  - heterostyly
KW  - Primula
KW  - supergene
KW  - gene duplication
KW  - neofunctionalization
Y1  - 2020
U6  - https://doi.org/10.1073/pnas.2006296117
SN  - 0027-8424
VL  - 117
IS  - 37
SP  - 23148
EP  - 23157
PB  - National Academy of Sciences
CY  - Washington
ER  - 
TY  - JOUR
A1  - Fujikura, Ushio
A1  - Jing, Runchun
A1  - Hanada, Atsushi
A1  - Takebayashi, Yumiko
A1  - Sakakibara, Hitoshi
A1  - Yamaguchi, Shinjiro
A1  - Kappel, Christian
A1  - Lenhard, Michael
T1  - Variation in splicing efficiency underlies morphological evolution in capsella
JF  - Developmental cell
N2  - Understanding the molecular basis of morphological change remains a central challenge in evolutionary-developmental biology. The transition from outbreeding to selfing is often associated with a dramatic reduction in reproductive structures and functions, such as the loss of attractive pheromones in hermaphroditic Caenorhabditis elegans and a reduced flower size in plants. Here, we demonstrate that variation in the level of the brassinosteroid-biosynthesis enzyme CYP724A1 contributes to the reduced flower size of selfing Capsella rubella compared with its outbreeding ancestor Capsella grandiflora. The primary transcript of the C. rubella allele is spliced more efficiently than that of C. grandiflora, resulting in higher brassinosteroid levels. These restrict organ growth by limiting cell proliferation. More efficient splicing of the C. rubella allele results from two de novo mutations in the selfing lineage. Thus, our results highlight the potentially widespread importance of differential splicing efficiency and higher-than-optimal hormone levels in generating phenotypic variation.
Y1  - 2017
U6  - https://doi.org/10.1016/j.devcel.2017.11.022
SN  - 1534-5807
SN  - 1878-1551
VL  - 44
IS  - 2
SP  - 192
EP  - 203
PB  - Cell Press
CY  - Cambridge
ER  - 
TY  - JOUR
A1  - Trost, Gerda
A1  - Vi, Son Lang
A1  - Czesnick, Hjördis
A1  - Lange, Peggy
A1  - Holton, Nick
A1  - Giavalisco, Patrick
A1  - Zipfel, Cyril
A1  - Kappel, Christian
A1  - Lenhard, Michael
T1  - Arabidopsis poly(A) polymerase PAPS1 limits founder-cell recruitment to organ primordia and suppresses the salicylic acid-independent immune response downstream of EDS1/PAD4
JF  - The plant journal
N2  - Polyadenylation of pre-mRNAs by poly(A) polymerase (PAPS) is a critical process in eukaryotic gene expression. As found in vertebrates, plant genomes encode several isoforms of canonical nuclear PAPS enzymes. In Arabidopsis thaliana these isoforms are functionally specialized, with PAPS1 affecting both organ growth and immune response, at least in part by the preferential polyadenylation of subsets of pre-mRNAs. Here, we demonstrate that the opposite effects of PAPS1 on leaf and flower growth reflect the different identities of these organs, and identify a role for PAPS1 in the elusive connection between organ identity and growth patterns. The overgrowth of paps1 mutant petals is due to increased recruitment of founder cells into early organ primordia, and suggests that PAPS1 activity plays unique roles in influencing organ growth. By contrast, the leaf phenotype of paps1 mutants is dominated by a constitutive immune response that leads to increased resistance to the biotrophic oomycete Hyaloperonospora arabidopsidis and reflects activation of the salicylic acid-independent signalling pathway downstream of ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1)/PHYTOALEXIN DEFICIENT4 (PAD4). These findings provide an insight into the developmental and physiological basis of the functional specialization amongst plant PAPS isoforms.
KW  - poly(A) polymerase
KW  - founder-cell recruitment
KW  - organ growth
KW  - polyadenylation
Y1  - 2014
U6  - https://doi.org/10.1111/tpj.12421
SN  - 0960-7412
SN  - 1365-313X
VL  - 77
IS  - 5
SP  - 688
EP  - 699
PB  - Wiley-Blackwell
CY  - Hoboken
ER  - 
TY  - JOUR
A1  - Kappel, Christian
A1  - Cuong Nguyen Huu, 
A1  - Lenhard, Michael
T1  - A short story gets longer: recent insights into the molecular basis of heterostyly
JF  - Journal of experimental botany
N2  - Heterostyly is a fascinating adaptation to promote outbreeding and a classical paradigm of botany. In the most common type of heterostyly, plants either form flowers with long styles and short stamens, or short styles and long stamens. This reciprocal organ positioning reduces pollen wastage and promotes cross-pollination, thus increasing male fitness. In addition, in many heterostylous species selfing and the generation of unfit progeny due to inbreeding depression is limited by a self-incompatibility system, thus promoting female fitness. The two floral forms are genetically determined by the S locus as a complex supergene, namely a chromosomal region containing several individual genes that control the different traits, such as style or stamen length, and are held together by very tight linkage due to suppressed recombination. Recent molecular-genetic studies in several systems, including Turnera, Fagopyrum, Linum, and Primula have begun to identify and characterize the causal heterostyly genes residing at the S locus. An emerging theme from several families is that the dominant S haplotype represents a hemizygous region not present on the recessive s haplotype. This provides an explanation for the suppressed recombination and suggests a scenario for the chromosomal evolution of the S locus. In this review, we discuss the results from recent molecular-genetic analyses in light of the classical models on the genetics and evolution of heterostyly.
KW  - CYP734A50
KW  - distyly
KW  - GLOBOSA2
KW  - hemizygosity
KW  - heterostyly
KW  - Primula
KW  - S locus
KW  - supergene
KW  - tristyly
Y1  - 2017
U6  - https://doi.org/10.1093/jxb/erx387
SN  - 0022-0957
SN  - 1460-2431
VL  - 68
SP  - 5719
EP  - 5730
PB  - Oxford Univ. Press
CY  - Oxford
ER  - 
TY  - GEN
A1  - Johnson, Kim L.
A1  - Ramm, Sascha
A1  - Kappel, Christian
A1  - Ward, Sally
A1  - Leyser, Ottoline
A1  - Sakamoto, Tomoaki
A1  - Kurata, Tetsuya
A1  - Bevan, Michael W.
A1  - Lenhard, Michael
T1  - The tinkerbell (tink) mutation identifies the dual-specificity MAPK phosphatase INDOLE- 3-BUTYRIC ACID-RESPONSE5 (IBR5) as a novel regulator of organ size in Arabidopsis
T2  - PLoS ONE
N2  - Mitogen-activated dual-specificity MAPK phosphatases are important negative regulators in the MAPK signalling pathways responsible for many essential processes in plants. In a screen for mutants with reduced organ size we have identified a mutation in the active site of the dual-specificity MAPK phosphatase INDOLE-3-BUTYRIC ACID-RESPONSE5 (IBR5) that we named tinkerbell (tink) due to its small size. Analysis of the tink mutant indicates that IBR5 acts as a novel regulator of organ size that changes the rate of growth in petals and leaves. Organ size and shape regulation by IBR5 acts independently of the KLU growth-regulatory pathway. Microarray analysis of tink/ibr5-6 mutants identified a likely role for this phosphatase in male gametophyte development. We show that IBR5 may influence the size and shape of petals through auxin and TCP growth regulatory pathways.
T3  - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 427 
KW  - class-i
KW  - protein phosphatase
KW  - auxin
KW  - responses
KW  - thaliana
KW  - kinase
KW  - growth
KW  - interacts
KW  - distinct
KW  - pathway
Y1  - 2018
U6  - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-410245
ER  - 
TY  - GEN
A1  - Huu, Cuong Nguyen
A1  - Plaschil, Sylvia
A1  - Himmelbach, Axel
A1  - Kappel, Christian
A1  - Lenhard, Michael
T1  - Female self-incompatibility type in heterostylous Primula is determined by the brassinosteroid-inactivating cytochrome P450 CYP734A50
T2  - Current biology
N2  - Most flowering plants are hermaphrodites, with flowers having both male and female reproductive organs. One widespread adaptation to limit self-fertilization is self-incompatibility (SI), where self-pollen fails to fertilize ovules.(1,2) In homomorphic SI, many morphologically indistinguishable mating types are found, although in heteromorphic SI, the two or three mating types are associated with different floral morphologies.(3-6) In heterostylous Primula, a hemizygous supergene determines a short-styled S-morph and a long-styled L-morph, corresponding to two different mating types, and full seed set only results from inter morph crosses.(7-9) Style length is controlled by the brassinosteroid (BR)-inactivating cytochrome P450 CYP734A50,(10) yet it remains unclear what defines the male and female incompatibility types. Here, we show that CYP734A50 also determines the female incompatibility type. Inactivating CYP734A50 converts short S-morph styles into long styles with the same incompatibility behavior as L-morph styles, and this effect can be mimicked by exogenous BR treatment. In vitro responses of S-and L-morph pollen grains and pollen tubes to increasing BR levels could only partly explain their different in vivo behavior, suggesting both direct and indirect effects of the different BR levels in S-versus L-morph stigmas and styles in controlling pollen performance. This BR-mediated SI provides a novel mechanism for preventing self-fertilization. The joint control of morphology and SI by CYP734A50 has important implications for the evolutionary buildup of the heterostylous syndrome and provides a straightforward explanation for why essentially all of the derived self-compatible homostylous Primula species are long homostyles.(11)
KW  - heteromorphic self-incompatibility
KW  - heterostyly
KW  - Primula forbesii
KW  - brassinosteroid
KW  - CYP734A50
KW  - supergene
KW  - pleiotropy
Y1  - 2022
U6  - https://doi.org/10.1016/j.cub.2021.11.046
SN  - 0960-9822
SN  - 1879-0445
VL  - 32
IS  - 3
SP  - 671
EP  - 676, E1-E5
PB  - Cell Press
CY  - Cambridge, Mass.
ER  - 
TY  - JOUR
A1  - Jöst, Moritz
A1  - Hensel, Goetz
A1  - Kappel, Christian
A1  - Druka, Arnis
A1  - Sicard, Adrien
A1  - Hohmann, Uwe
A1  - Beier, Sebastian
A1  - Himmelbach, Axel
A1  - Waugh, Robbie
A1  - Kumlehn, Jochen
A1  - Stein, Nils
A1  - Lenhard, Michael
T1  - The INDETERMINATE DOMAIN Protein BROAD LEAF1 Limits Barley Leaf Width by Restricting Lateral Proliferation
JF  - Current biology
N2  - Variation in the size, shape, and positioning of leaves as the major photosynthetic organs strongly impacts crop yield, and optimizing these aspects is a central aim of cereal breeding [1, 2]. Leaf growth in grasses is driven by cell proliferation and cell expansion in a basal growth zone [3]. Although several factors influencing final leaf size and shape have been identified from rice and maize [4-14], what limits grass leaf growth in the longitudinal or transverse directions during leaf development remains poorly understood. To identify factors involved in this process, we characterized the barley mutant broad leaf1 (blf1). Mutants form wider but slightly shorter leaves due to changes in the numbers of longitudinal cell files and of cells along the leaf length. These differences arise during primordia outgrowth because of more cell divisions in the width direction increasing the number of cell files. Positional cloning, analysis of independent alleles, and transgenic complementation confirm that BLF1 encodes a presumed transcriptional regulator of the INDETERMINATE DOMAIN family. In contrast to loss-of-function mutants, moderate overexpression of BLF1 decreases leaf width below wild-type levels. A functional BLF1-vYFP fusion protein expressed from the endogenous promoter shows a dynamic expression pattern in the shoot apical meristem and young leaf primordia. Thus, we propose that the BLF1 gene regulates barley leaf size by restricting cell proliferation in the leaf-width direction. Given the agronomic importance of canopy traits in cereals, identifying functionally different BLF1 alleles promises to allow for the generation of optimized cereal ideotypes.
Y1  - 2016
U6  - https://doi.org/10.1016/j.cub.2016.01.047
SN  - 0960-9822
SN  - 1879-0445
VL  - 26
SP  - 903
EP  - 909
PB  - Cell Press
CY  - Cambridge
ER  - 
TY  - JOUR
A1  - Cuong Nguyen Huu, 
A1  - Kappel, Christian
A1  - Keller, Barbara
A1  - Sicard, Adrien
A1  - Takebayashi, Yumiko
A1  - Breuninger, Holger
A1  - Nowak, Michael D.
A1  - Bäurle, Isabel
A1  - Himmelbach, Axel
A1  - Burkart, Michael
A1  - Ebbing-Lohaus, Thomas
A1  - Sakakibara, Hitoshi
A1  - Altschmied, Lothar
A1  - Conti, Elena
A1  - Lenhard, Michael
T1  - Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses
JF  - eLife
N2  - Heterostyly is a wide-spread floral adaptation to promote outbreeding, yet its genetic basis and evolutionary origin remain poorly understood. In Primula (primroses), heterostyly is controlled by the S-locus supergene that determines the reciprocal arrangement of reproductive organs and incompatibility between the two morphs. However, the identities of the component genes remain unknown. Here, we identify the Primula CYP734A50 gene, encoding a putative brassinosteroid-degrading enzyme, as the G locus that determines the style-length dimorphism. CYP734A50 is only present on the short-styled S-morph haplotype, it is specifically expressed in S-morph styles, and its loss or inactivation leads to long styles. The gene arose by a duplication specific to the Primulaceae lineage and shows an accelerated rate of molecular evolution. Thus, our results provide a mechanistic explanation for the Primula style-length dimorphism and begin to shed light on the evolution of the S-locus as a prime model for a complex plant supergene.
Y1  - 2016
U6  - https://doi.org/10.7554/eLife.17956
SN  - 2050-084X
VL  - 5
PB  - eLife Sciences Publications
CY  - Cambridge
ER  - 
TY  - JOUR
A1  - Kappel, Christian
A1  - Illing, Nicola
A1  - Huu, Cuong Nguyen
A1  - Barger, Nichole N.
A1  - Cramer, Michael D.
A1  - Lenhard, Michael
A1  - Midgley, Jeremy J.
T1  - Fairy circles in Namibia are assembled from genetically distinct grasses
JF  - Communications biology
N2  - Fairy circles are striking regularly sized and spaced, bare circles surrounded by Stipagrostis grasses that occur over thousands of square kilometres in Namibia. The mechanisms explaining their origin, shape, persistence and regularity remain controversial. One hypothesis for the formation of vegetation rings is based on the centrifugal expansion of a single individual grass plant, via clonal growth and die-back in the centre. Clonality could explain FC origin, shape and long-term persistence as well as their regularity, if one clone competes with adjacent clones. Here, we show that for virtually all tested fairy circles the periphery is not exclusively made up of genetically identical grasses, but these peripheral grasses belong to more than one unrelated genet. These results do not support a clonal explanation for fairy circles. Lack of clonality implies that a biological reason for their origin, shape and regularity must emerge from competition between near neighbor individuals within each fairy circle. Such lack of clonality also suggests a mismatch between longevity of fairy circles versus their constituent plants. Furthermore, our findings of lack of clonality have implications for some models of spatial patterning of fairy circles that are based on self-organization. Christian Kappel et al. examine the genetic composition of fairy circles, regular circular patterns of grasses in the Namib Desert, using ddRAD-seq. They find that these grasses are made up of multiple unrelated genets rather than genetically identical grasses, suggesting non-clonality.
Y1  - 2020
U6  - https://doi.org/10.1038/s42003-020-01431-0
SN  - 2399-3642
VL  - 3
IS  - 1
PB  - Springer Nature
CY  - London
ER  -