scholarly journals Recruitment of an ancient branching program to suppress carpel development in maize flowers

2021 ◽  
Author(s):  
Harry Klein ◽  
Joseph Gallagher ◽  
Edgar Demesa-Arevalo ◽  
María Jazmín Abraham-Juárez ◽  
Michelle Heeney ◽  
...  

AbstractFloral morphology is immensely diverse. One developmental process acting to shape this diversity is growth suppression. For example, grass flowers exhibit extreme diversity in floral sexuality, arising through differential suppression of stamens or carpels. In maize, carpels undergo programmed cell death in half of the flowers initiated in ears and in all flowers in tassels. The HD-ZIP I transcription factor gene GRASSY TILLERS1 (GT1) is one of only a few genes known to regulate this process. To identify additional regulators of carpel suppression, we performed a gt1 enhancer screen, and found a genetic interaction between gt1 and ramosa3 (ra3). RA3 is a classic inflorescence meristem determinacy gene that encodes a trehalose-6-phosphate (T6P) phosphatase (TPP). Dissection of floral development revealed that ra3 single mutants have partially derepressed carpels, whereas gt1; ra3 double mutants have completely derepressed carpels. Surprisingly, gt1 suppresses ra3 inflorescence branching, revealing a role for gt1 in meristem determinacy. Supporting these genetic interactions, GT1 and RA3 proteins colocalize to carpel nuclei in developing flowers. Global expression profiling revealed common genes misregulated in single and double mutant flowers, as well as in derepressed gt1 axillary meristems. Indeed, we found that ra3 enhances gt1 vegetative branching, similar to the roles for the trehalose pathway and GT1 homologs in the eudicots. This functional conservation over ~160 million years of evolution reveals ancient roles for GT1-like genes and the trehalose pathway in regulating axillary meristem suppression, later recruited to mediate carpel suppression. Our findings expose hidden pleiotropy of classic maize genes, and show how an ancient developmental program was redeployed to sculpt floral form.

2022 ◽  
Vol 119 (2) ◽  
pp. e2115871119
Author(s):  
Harry Klein ◽  
Joseph Gallagher ◽  
Edgar Demesa-Arevalo ◽  
María Jazmín Abraham-Juárez ◽  
Michelle Heeney ◽  
...  

Carpels in maize undergo programmed cell death in half of the flowers initiated in ears and in all flowers in tassels. The HD-ZIP I transcription factor gene GRASSY TILLERS1 (GT1) is one of only a few genes known to regulate this process. To identify additional regulators of carpel suppression, we performed a gt1 enhancer screen and found a genetic interaction between gt1 and ramosa3 (ra3). RA3 is a classic inflorescence meristem determinacy gene that encodes a trehalose-6-phosphate (T6P) phosphatase (TPP). Dissection of floral development revealed that ra3 single mutants have partially derepressed carpels, whereas gt1;ra3 double mutants have completely derepressed carpels. Surprisingly, gt1 suppresses ra3 inflorescence branching, revealing a role for gt1 in meristem determinacy. Supporting these genetic interactions, GT1 and RA3 proteins colocalize to carpel nuclei in developing flowers. Global expression profiling revealed common genes misregulated in single and double mutant flowers, as well as in derepressed gt1 axillary meristems. Indeed, we found that ra3 enhances gt1 vegetative branching, similar to the roles for the trehalose pathway and GT1 homologs in the eudicots. This functional conservation over ∼160 million years of evolution reveals ancient roles for GT1-like genes and the trehalose pathway in regulating axillary meristem suppression, later recruited to mediate carpel suppression. Our findings expose hidden pleiotropy of classic maize genes and show how an ancient developmental program was redeployed to sculpt floral form.


2017 ◽  
Author(s):  
Jamie L. Kostyun ◽  
Jill C. Preston ◽  
Leonie C. Moyle

AbstractBackgroundHeterochronic shifts during mid to late stages of organismal development have been proposed as key mechanisms generating phenotypic diversity. To determine whether late heterochronic shifts underlie derived floral morphologies within Jaltomata (Solanaceae) – a genus whose species have extensive and recently evolved floral diversity – we compared floral development of four diverse species (including an ambiguously ancestral or secondarily derived rotate, two putatively independently evolved campanulate, and a tubular morph) to the ancestral rotate floral form, as well as to an outgroup that shares this ancestral floral morphology.ResultsWe determined that early floral development (<1 mm bud diameter, corresponding to completion of organ whorl initiation) is very similar among all species, but that different mature floral forms are distinguishable by mid-development (>1 mm diameters) due to differential growth acceleration of corolla traits. Floral ontogeny among similar mature rotate forms remains comparable until late stages, while somewhat different patterns of organ growth are found between species with similar campanulate forms.ConclusionsOur data suggest shared floral patterning during early-stage development, but that different heterochronic shifts during mid- and late-stage development contributes to divergent floral traits. Heterochrony thus appears to have been important in the rapid and repeated diversification of Jaltomata flowers.


Development ◽  
2000 ◽  
Vol 127 (6) ◽  
pp. 1267-1276 ◽  
Author(s):  
P.D. Jenik ◽  
V.F. Irish

The shoot apical meristem of Arabidopsis thaliana consists of three cell layers that proliferate to give rise to the aerial organs of the plant. By labeling cells in each layer using an Ac-based transposable element system, we mapped their contributions to the floral organs, as well as determined the degree of plasticity in this developmental process. We found that each cell layer proliferates to give rise to predictable derivatives: the L1 contributes to the epidermis, the stigma, part of the transmitting tract and the integument of the ovules, while the L2 and L3 contribute, to different degrees, to the mesophyll and other internal tissues. In order to test the roles of the floral homeotic genes in regulating these patterns of cell proliferation, we carried out similar clonal analyses in apetala3-3 and agamous-1 mutant plants. Our results suggest that cell division patterns are regulated differently at different stages of floral development. In early floral stages, the pattern of cell divisions is dependent on position in the floral meristem, and not on future organ identity. Later, during organogenesis, the layer contributions to the organs are controlled by the homeotic genes. We also show that AGAMOUS is required to maintain the layered structure of the meristem prior to organ initiation, as well as having a non-autonomous role in the regulation of the layer contributions to the petals.


2021 ◽  
Author(s):  
Aniket Sengupta ◽  
Lena C. Hileman

Abstract BackgroundAn outstanding question in evolutionary biology is how genetic interactions defining novel traits evolve. They may evolve either by de novo assembly of previously non-interacting genes or by en bloc co-option of interactions from other functions. We tested these hypotheses in the context of a novel phenotype—Lamiales flower monosymmetry—defined by a developmental program that relies on regulatory interaction among CYCLOIDEA , RADIALIS , DIVARICATA , and DRIF gene products. In Antirrhinum majus (snapdragon), representing Lamiales, we tested whether components of this program likely function beyond their previously known role in petal and stamen development. In Solanum lycopersicum (tomato), representing Solanales which diverged from Lamiales before the origin of Lamiales floral monosymmetry, we additionally tested for regulatory interactions in this program. ResultsWe found that RADIALIS , DIVARICATA , and DRIF are expressed in snapdragon ovaries and developing fruit, similar to their homologs during tomato fruit development. Additionally, we found that a tomato CYCLOIDEA ortholog positively regulates a tomato RADIALIS ortholog. ConclusionOur results provide preliminary support to the hypothesis that the developmental program defining floral monosymmetry in Lamiales was co-opted en bloc from a function in carpel development. This expands our understanding of novel trait evolution facilitated by co-option of existing regulatory interactions.


Author(s):  
Maxim S Nuraliev ◽  
Sophia V Yudina ◽  
Ekaterina A Shepeleva ◽  
Ba Vuong Truong ◽  
Thi Xuyen Do ◽  
...  

Abstract Thismia is characterized by an exceptionally complicated floral morphology that is currently not understood properly. In the taxonomic literature, descriptive rather than morphological terms are often applied to parts of the flower in Thismia, relating to the general appearance of the floral organs instead of their precise homologies. Precise understanding of the floral structure is complicated by the rarity of Thismia spp. and the paucity of appropriate material. Here we provide a comprehensive study of reproductive organs of three Thismia spp. (T. annamensis, T. javanica and T. mucronata) including the first investigation of inflorescence architecture and early floral development in Thismiaceae. We found a hitherto unknown diversity of the reproductive shoots in the genus, manifested in the number of floral prophylls (two or three, in contrast to a single prophyll in the vast majority of monocots) and in the branching plane resulting in two distinct inflorescence types, a drepanium and a bostryx. We report the non-acropetal sequence of initiation of floral whorls (with stamens being the last elements to initiate), never previously described in monocots, and the gynoecium composed of completely plicate carpels, also a rare feature for monocots. Floral vasculature is relatively uniform in Thismia, but significant interspecific differences are found in tepal innervation, including the number of tepal traces; some of these differences are not immediately related to the external tepal morphology. We argue that the annulus, which acts as a roof of the hypanthium, possesses an androecium nature and represents congenitally fused bases of stamen filaments. We describe the stamens as laminar structures, which are also shortly tubular in the distal part of the supraconnective with the adaxial tubular side forming a skirt-like appendage. Finally, the placentas, which are column-like when mature, are initially parietal, becoming secondarily similar to free-central placentas through schizogenous separation from the ovary wall.


Botany ◽  
2015 ◽  
Vol 93 (1) ◽  
pp. 47-56 ◽  
Author(s):  
Letícia Peres Poli ◽  
Lívia Godinho Temponi ◽  
Alessandra Ike Coan

Studies on floral development have widened the knowledge on the floral morphology of Araceae, particularly in genera delimited through classical taxonomic treatments. In Pothoideae, floral ontogenetic studies are limited to some representatives of Pothoidium Schott and Pothos L. and only one species of Anthurium Schott, with no focus on gynoecium. This background reveals a lack of ontogenetic data on the largest genus in the clade. This paper presents gynoecial ontogeny of species circumscribed in different sections of Anthurium, describes gynoecial developmental patterns, and evaluates the relevance of ontogenetic characteristics in the taxonomy of the sections studied. New data for the Araceae include the recognition of four floral developmental phases, the carpellary nature of the ovarian septum, and the development of the symplicate and synascidiate zones of the gynoecium. The apical septum described in Anthurium scandens (Aubl.) Engl. is first reported for the genus in this study. We also highlight the importance of these ontogenetic data as new information for the Pothoideae within Araceae and to understand the notable phases of floral development in the reproductive biology of Anthurium.


1999 ◽  
Vol 124 (3) ◽  
pp. 296-300 ◽  
Author(s):  
Renate Karle ◽  
Thomas H. Boyle

The effects of floral morphology and breeding behavior on flower longevity were investigated in Easter cactus [Hatiora ×graeseri (Werderm.) Barthlott)]. Four clones were studied: two diploid (n = 11) clones (`Evita' and `Purple Pride') that were highly self-incompatible (SI), and two cytochimeras (diploid epidermis and tetraploid subepidermis) that were recovered from the diploid cultivars, both of which were self-compatible (SC). The clones exhibited differences in the stage of floral development in which autogamy commenced. Autogamy commenced on the day of anthesis in the two `Evita' clones and occurred ≈5 days after anthesis in the `Purple Pride' cytochimera. In the `Purple Pride' diploid clone, anthers and stigmatic lobes remained spatially separated during the period from anthesis to senescence. Examination of styles collected from senesced, undisturbed flowers showed that few pollen tubes traversed to the base of the styles for the two SI diploid clones, whereas large numbers of pollen tubes were present at the base of the styles for the two SC cytochimeras. Flower longevity for the `Evita' cytochimera was significantly less than for `Evita' diploid, but the diploid and cytochimeral clones of `Purple Pride' exhibited similar flower longevities. Application of 2 mm silver thiosulfate, an inhibitor of ethylene (C2H4) action, did not affect flower longevity of `Evita' cytochimera. Our results show that flower longevity in Easter cactus is influenced by breeding behavior and the stage of floral development at which autogamy commences.


1998 ◽  
Vol 180 (17) ◽  
pp. 4628-4637 ◽  
Author(s):  
Anthony G. Garza ◽  
Jeffrey S. Pollack ◽  
Baruch Z. Harris ◽  
Albert Lee ◽  
Ingrid M. Keseler ◽  
...  

ABSTRACT Myxococcus xanthus cells carrying the Ω4408 Tn5lac insertion at the sde locus show defects in fruiting body development and sporulation. Our analysis ofsde expression patterns showed that this locus is induced early in the developmental program (0 to 2 h) and that expression increases approximately fivefold after 12 h of development. Further studies showed that expression of sde is induced as growing cells enter stationary phase, suggesting that activation of thesde locus is not limited to the developmental process. Because the peak levels of sde expression in both ansde + and an sde mutant background were similar, we conclude that the sde locus is not autoregulated. Characterization of the sde locus by DNA sequence analysis indicated that the Ω4408 insertion occurred within the sdeK gene. Primer extension analyses localized the 5′ end of sde transcript to a guanine nucleotide 307 bp upstream of the proposed start for the SdeK coding sequence. The DNA sequence in the −12 and −24 regions upstream of the sdetranscriptional start site shows similarity to the ς54family of promoters. The results of complementation studies suggest that the defects in development and sporulation caused by the Ω4408 insertion are due to an inactivation of sdeK. The predicted amino acid sequence of SdeK was found to have similarity to the sequences of the histidine protein kinases of two-component regulatory systems. Based on our results, we propose that SdeK may be part of a signal transduction pathway required for the activation and propagation of the early developmental program.


2019 ◽  
Vol 70 (9) ◽  
pp. 781 ◽  
Author(s):  
Jialin Guo ◽  
Gaisheng Zhang ◽  
Yulong Song ◽  
Shoucai Ma ◽  
Na Niu ◽  
...  

Multi-ovary wheat is a unique variety of wheat that has one to three pistils and three stamens, and can stably set one to three grains in each floret. By observing the developmental process of additional pistils, we found that the additional pistil was derived from a protrusion generated at the base of the main pistil, between the frontal stamen and lateral stamen. The additional pistil’s development was greatly delayed compared with the main pistil at an early stage. However, after the awn exposed stage, it developed very rapidly to a mature pistil within the maturity time of the main pistil. Generally, the grains originating from additional pistils were smaller than the grains from the main pistil. By studying the penetrance and germination conditions of multi-ovary wheat, we found that no matter which ovary the grains originated from, they had the same penetrance. However, the germination ability of grains generated from the main pistil was significantly higher than that of grains from additional pistils. Our results showed that multi-ovary wheat was an excellent variety, not only for studying the mechanisms of the multi-ovary trait and floral development in wheat, but also for improving the propagation coefficient and promoting the progress of wheat breeding. This paper lays a theoretical foundation for the practical application of multi-ovary trait in hybrid wheat; our results could be implemented in fostering future breeding activities focussed on the development of high yield wheat cultivars.


1983 ◽  
Vol 31 (6) ◽  
pp. 585 ◽  
Author(s):  
CA McConchie

Floral development of Maidenia rubra was followed from initiation to maturity. Plants are dioecious. Both male and female inflorescences develop from complexes initiated subapically. Complexes have three meristematic components that include two inflorescence initials flanking a central primordium; these form sequentially in the axil of the preceding initial. The third component also produces an inflorescence and branches sympodially to form further floral initials that have a spiral arrangement. The female inflorescences produce a single flower only with an inferior, unilocular ovary and three sepals, staminodes and bifid stigma. In the locule, numerous bitegmic ovules, borne panetally, are produced. A male inflorescence produces hundreds of small flowers that are released and float to the surface individually. Each male flower has three sepals, a staminode and two stamens, each anther consisting of three locules with eight pollen grains. Prior to maturation, the anther wall breaks down leaving a membraneous layer that assists in binding the octad of pollen grains together. Both male and female inflorescences are enclosed in a pair of fused bracts. The floral morphology is compared with other closely related genera in the Hydrocharitaceae and the unique features are assessed.


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