Seasonal changes in day length influence flowering time in many plant species. In
Arabidopsis, flowering is accelerated by exposure to long day (LD). Those inductive photoperiods are perceived in ...leaves
1 and initiate a long-distance signaling mediated by CO and FT.
CO is expressed in the phloem according to a circadian rhythm
2–4. Only under LD does CO induce
FT expression as high levels of
CO in the evening coincide with the external light that stabilizes CO protein
4, 5. Subsequently, FT protein travels through the phloem to the shoot apex where, together with FD, it initiates flowering
6–12. Despite the photoperiodic induction, a mechanism of floral repression is needed to avoid precocious flowering. We show that
TEMPRANILLO genes (
TEM1 and
TEM2) act as novel direct
FT repressors. Molecular and genetic analyses suggest that a quantitative balance between the activator CO and the repressor TEM determines
FT levels. Moreover, developmental
TEM downregulation marks the timing of flowering, as it shifts the CO/TEM balance in favor of CO activity, allowing
FT transcript to reach the threshold level required to trigger flowering. We envision that this might be a general mechanism between long-day plants to ensure a tight regulation of flowering time.
Fluctuations in environmental conditions greatly influence life on earth. Plants, as sessile organisms, have developed molecular mechanisms to adapt their development to changes in daylength, or ...photoperiod. One of the first plant features that comes to mind as affected by the duration of the day is flowering time; we all bring up a clear image of spring blossom. However, for many plants flowering happens at other times of the year, and many other developmental aspects are also affected by changes in daylength, which range from hypocotyl elongation in
to tuberization in potato or autumn growth cessation in trees. Strikingly, many of the processes affected by photoperiod employ similar gene networks to respond to changes in the length of light/dark cycles. In this review, we have focused on developmental processes affected by photoperiod that share similar genes and gene regulatory networks.
Summary
The effective anti‐malarial drug artemisinin (AN) isolated from Artemisia annua is relatively expensive due to the low AN content in the plant as AN is only synthesized within the glandular ...trichomes. Therefore, genetic engineering of A. annua is one of the most promising approaches for improving the yield of AN. In this work, the AaMYB1 transcription factor has been identified and characterized. When AaMYB1 is overexpressed in A. annua, either exclusively in trichomes or in the whole plant, essential AN biosynthetic genes are also overexpressed and consequently the amount of AN is significantly increased. Artemisia AaMYB1 constitutively overexpressing plants displayed a greater number of trichomes. In order to study the role of AaMYB1 on trichome development and other possibly connected biological processes, AaMYB1 was overexpressed in Arabidopsis thaliana. To support our findings in Arabidopsis thaliana, an AaMYB1 orthologue from this model plant, AtMYB61, was identified and atmyb61 mutants characterized. Both AaMYB1 and AtMYB61 affected trichome initiation, root development and stomatal aperture in A. thaliana. Molecular analyses indicated that two crucial trichome activator genes are misexpressed in atmyb61 mutant plants and in plants overexpressing AaMYB1. Furthermore, AaMYB1 and AtMYB61 are also essential for gibberellin (GA) biosynthesis and degradation in both species by positively affecting the expression of the enzymes that convert GA9 into the bioactive GA4 as well as the enzymes involved in the degradation of GA4. Overall, these results identify AaMYB1/AtMYB61 as a key component of the molecular network that connects important biosynthetic processes, and reveal its potential value for AN production through genetic engineering.
Significance Statement
The biosynthetic pathway of artemisinin, an antimalarial and anticancer substance, only takes place in Artemisia annua glandular trichomes; however artemisinin content in this plant is too low to cover worldwide demand for the product. New research has identified AaMYB1 transcription factor that positively affects not only AN biosynthesis but also, as its orthologue AtMYB61, affect gibberellin biosynthesis and trichome proliferation; two diverse but connected processes necessary for improving AN yield in planta.
The ABC model of flower organ identity is widely recognized as providing a framework for understanding the specification of flower organs in diverse plant species 1. Recent studies in Arabidopsis ...thaliana have shown that three closely related MADS-box genes, SEPALLATA1 (SEP1), SEP2 and SEP3, are required to specify petals, stamens, and carpels because these organs are converted into sepals in sep1 sep2 sep3 triple mutants 3, 4. Additional studies indicate that the SEP proteins form multimeric complexes with the products of the B and C organ identity genes. Here, we characterize the SEP4 gene, which shares extensive sequence similarity to and an overlapping expression pattern with the other SEP genes. Although sep4 single mutants display a phenotype similar to that of wild-type plants, we find that floral organs are converted into leaf-like organs in sep1 sep2 sep3 sep4 quadruple mutants, indicating the involvement of all four SEP genes in the development of sepals. We also find that SEP4 contributes to the development of petals, stamens, and carpels in addition to sepals and that it plays an important role in meristem identity. These and other data demonstrate that the SEP genes play central roles in flower meristem identity and organ identity.
The Arabidopsis fruit forms a seedpod that develops from the fertilized gynoecium. It is mainly comprised of an ovary in which three distinct tissues can be differentiated: the valves, the valve ...margins and the replum. Separation of cells at the valve margin allows for the valves to detach from the replum and thus dispersal of the seeds. Valves and valve margins are located in lateral positions whereas the replum is positioned medially and retains meristematic properties resembling the shoot apical meristem (SAM). Members of the WUSCHEL‐related homeobox family have been involved in stem cell maintenance in the SAM, and within this family, we found that WOX13 is expressed mainly in meristematic tissues including the replum. We also show that wox13 loss‐of‐function mutations reduce replum size and enhance the phenotypes of mutants affected in the replum identity gene RPL. Conversely, misexpression of WOX13 produces, independently from BP and RPL, an oversized replum and valve defects that closely resemble those of mutants in JAG/FIL activity genes. Our results suggest that WOX13 promotes replum development by likely preventing the activity of the JAG/FIL genes in medial tissues. This regulation seems to play a role in establishing the gradient of JAG/FIL activity along the medio‐lateral axis of the fruit critical for proper patterning. Our data have allowed us to incorporate the role of WOX13 into the regulatory network that orchestrates fruit patterning.
The long juvenile period of fruit trees makes their breeding costly and time-consuming. Therefore, flowering time engineering and shortening the juvenile phase have become a breeding priority for the ...genetic improvement of fruit tree crops. Many economically valuable fruit trees belong to the Rosaceae family including apples and strawberries. TEMPRANILLO (TEM) acts as a key player in flowering time control through inhibiting FT function. Two genes with high sequence similarity with the Arabidopsis TEM genes were isolated from apple (Malus domestica). Due to the complexity of carrying out functional studies in apple, we characterized their function in woodland strawberry as well as their expression in apple. The expression of MdTEM genes in apple tissues from juvenile plants was dramatically higher than that in the tissues from adult trees. In woodland strawberry, the overexpression of MdTEM genes down-regulated FvFT1, FvGA3OX1, and FvGA3OX2 genes in strawberry. The MdTEM-overexpressing lines exhibited delayed flowering, in terms of days to flowering and the number of leaves at flowering. While, RNAi-mediated silencing of TEM resulted in five days earlier flowering, with a lower number of leaves, a higher trichome density, and in some cases, caused in vitro flowering. According to these results and in silico analyses, it can be concluded that MdTEM1 and MdTEM2 can be considered as orthologs of FvTEM and probably AtTEM genes, which play an important role in regulating the juvenile phase and flowering time through regulating FT and GA biosynthetic pathway.
Summary
In the age‐dependent pathway, microRNA 156 (miR156) is essential for the correct timing of developmental transitions. miR156 negatively regulates several SPL genes, which promote the ...juvenile‐to‐adult and floral transitions in part through upregulation of miR172. The transcriptional repressors TEMPRANILLO1 (TEM1) and TEM2 delay flowering in Arabidopsis thaliana at least through direct repression of FLOWERING LOCUS T (FT) and gibberellin biosynthetic genes, and have also been reported to participate in the length of the juvenile phase. Levels of TEM mRNA and miR156 decrease gradually, allowing progression through developmental phases. Given these similarities, we hypothesized that TEMs and the miR156/SPL/miR172 module could act through a common genetic pathway. We analyzed the effect of TEMs on levels of miR156, SPL and miR172, tested binding of TEMs to these genes using chromatin immunoprecipitation and analyzed the genetic interaction between TEMs and miR172. We found that TEMs played a stronger role in the floral transition than in the juvenile‐to‐adult transition. TEM1 repressed MIR172A, MIR172B and MIR172C expressions and bound in vivo to at least MIR172C sequences. Genetic analyses indicated that TEMs affect the regulation of developmental timing through miR172.
Significance Statement
The timing of plant developmental transitions is essential for adequate growth and adaptation to environmental conditions. First, young plants undergo a juvenile‐to‐adult transition then become competent to flower. Afterwards, the floral transition promotes the production of flowers and, consequently, the reproduction of the species. In this work we found that the TEMPRANILLO floral repressors act in the age‐dependent developmental pathway that is responsible for the juvenile‐to‐adult transition and flowering, in part through direct regulation of microRNA 172.
Abnormal flowers have been recognized for thousands of years, but only in the past decade have the mysteries of flower development begun to unfold. Among these mysteries is the differentiation of ...four distinct organ types (sepals, petals, stamens and carpels), each of which may be a modified leaf. A landmark accomplishment in plant developmental biology is the ABC model of flower organ identity. This simple model provides a conceptual framework for explaining how the individual and combined activities of the ABC genes produce the four organ types of the typical eudicot flower. Here we show that the activities of the B and C organ-identity genes require the activities of three closely related and functionally redundant MADS-box genes, SEPALLATA1/2/3 (SEP1/2/3). Triple mutant Arabidopsis plants lacking the activity of all three SEP genes produce flowers in which all organs develop as sepals. Thus SEP1/2/3 are a class of organ-identity genes that is required for development of petals, stamens and carpels.
Elucidating molecular links between cell‐fate regulatory networks and dynamic patterning modules is a key for understanding development. Auxin is important for plant patterning, particularly in ...roots, where it establishes positional information for cell‐fate decisions. PIN genes encode plasma membrane proteins that serve as auxin efflux transporters; mutations in members of this gene family exhibit smaller roots with altered root meristems and stem‐cell patterning. Direct regulators of PIN transcription have remained elusive. Here, we establish that a MADS‐box gene (XAANTAL2, XAL2/AGL14) controls auxin transport via PIN transcriptional regulation during Arabidopsis root development; mutations in this gene exhibit altered stem‐cell patterning, root meristem size, and root growth. XAL2 is necessary for normal shootward and rootward auxin transport, as well as for maintaining normal auxin distribution within the root. Furthermore, this MADS‐domain transcription factor upregulates PIN1 and PIN4 by direct binding to regulatory regions and it is required for PIN4‐dependent auxin response. In turn, XAL2 expression is regulated by auxin levels thus establishing a positive feedback loop between auxin levels and PIN regulation that is likely to be important for robust root patterning.
The XAL2/AGL14 transcription factor regulates the expression of several members of the auxin efflux family to control auxin gradients and root development in Arabidopsis.
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