Genetic control of branching is a primary determinant of yield, regulating seed number and harvesting ability, yet little is known about the molecular networks that shape grain-bearing inflorescences of cereal crops. Here, we used the maize (Zea mays) inflorescence to investigate gene networks that modulate determinacy, specifically the decision to allow branch growth. We characterized developmental transitions by associating spatiotemporal expression profiles with morphological changes resulting from genetic perturbations that disrupt steps in a pathway controlling branching. Developmental dynamics of genes targeted in vivo by the transcription factor RAMOSA1, a key regulator of determinacy, revealed potential mechanisms for repressing branches in distinct stem cell populations, including interactions with KNOTTED1, a master regulator of stem cell maintenance. Our results uncover discrete developmental modules that function in determining grass-specific morphology and provide a basis for targeted crop improvement and translation to other cereal crops with comparable inflorescence architectures.
Plant development depends on the activity of various types of meristems that generate organs such as leaves and floral organs throughout the life cycle. Grass species produce complex inflorescences and unique flowers. The grass inflorescence is composed of different types of branches, including a specialized branch called a spikelet. The spikelet is a special unit of the inflorescence and forms one to several florets, depending on the species. In the floret, floral organs such as perianth organs, carpels and stamens are formed. In Arabidopsis, because the inflorescence meristem (IM) forms the floral meristems (FMs) directly on its flanks, the change of meristem fate is relatively simple. In contrast, in grasses, different types of meristem, such as the IM, the branch meristem (BM), the spikelet pair meristem (SPM) in some grasses, the spikelet meristem (SM) and the FM, are responsible for the elaboration of their complex inflorescences and flowers. Therefore, sequential changes of meristem fate are required, and a number of genes involved in the specification of the fate of each meristem have been identified. In this review, we focus on the following issues concerning the fate of the reproductive meristems in two grass species, maize (Zea mays) and rice (Oryza sativa): (i) meristem regulation during inflorescence development; (ii) specification and fate change of the BM and the SM; (iii) determinacy of the FM; and (iv) communication between the meristem and lateral organs.
Plant architecture is dictated by precise control of meristematic activity. In the shoot, an imbalance in positive or negative maintenance signals can result in a fasciated or enlarged meristem phenotype. fasciated ear4 (fea4) is a semidwarfed mutant with fasciated ears and tassels as well as greatly enlarged vegetative and inflorescence meristems. We identified FEA4 as a bZIP transcription factor, orthologous to Arabidopsis thaliana PERIANTHIA. FEA4 was expressed in the peripheral zone of the vegetative shoot apical meristem and in the vasculature of immature leaves and conspicuously excluded from the stem cell niche at the tip of the shoot apical meristem and from incipient leaf primordia. Following the transition to reproductive fate, FEA4 was expressed throughout the entire inflorescence and floral meristems. Native expression of a functional YFP:FEA4 fusion recapitulated this pattern of expression. We used chromatin immunoprecipitation-sequencing to identify 4060 genes proximal to FEA4 binding sites, including ones that were potentially bound and modulated by FEA4 based on transcriptional changes in fea4 mutant ears. Our results suggest that FEA4 promotes differentiation in the meristem periphery by regulating auxin-based responses and genes associated with leaf differentiation and polarity, potentially in opposition to factors such as KNOTTED1 and WUSCHEL.
The vegetative and reproductive shoot architectures displayed by members of the grass family are critical to reproductive success, and thus agronomic yield. Variation in shoot architecture is explained by the maintenance, activity and determinacy of meristems, pools of pluripotent stem cells responsible for post-embryonic plant growth. This review summarizes recent progress in understanding the major properties of grass shoot meristems, focusing on vegetative phase meristems and the floral transition, primarily in rice and maize. Major areas of interest include: the control of meristem homeostasis by the CLAVATA-WUSCHEL pathway and by hormones such as cytokinin; the initiation of axillary meristems and the control of axillary meristem dormancy; and the environmental and endogenous cues that regulate flowering time. In an accompanying paper, Tanaka et al. review subsequent stages of shoot development, including current knowledge of reproductive meristem determinacy and the fate transitions associated with these meristems.
Roots encounter a plethora of microorganisms in the soil environment that are either deleterious, neutral, or beneficial to plant growth. Root endophytic fungi are ubiquitous. These include dark septate endophytes whose role in plant growth and the maintenance of plant communities is largely unknown. The objectives of this review were to assess the structural features of the interactions between dark septate endophytic fungi and the roots of both angiopsperms and conifers, and to suggest avenues for further research. Several light microscopy studies of endophyte-root interactions have revealed a variety of structural features, depending on host species and plant growth conditions. In some cases, when fungal hyphae enter roots they cause cell breakdown, whereas in other situations there is little noticeable effect. In some tree species, associations with these endophytes may mimic ectomycorrhizas or ectendomycorrhizas. The few ultrastructural studies indicate that intracellular hyphae lack a host-derived perifungal membrane and interfacial matrix material, features typical of biotrophic fungus -plant cell interactions. This raises questions concerning nutrient exchange between these fungi and plant cells. Further research in this area is needed. New approaches that include molecular cytology and livecell imaging are needed to determine early changes in plant cells when challenged with these fungi.Résumé : Dans l'environnement édaphique, les racines rencontrent une pléthore de microorganismes néfastes, neutres ou bénéfiques à la croissance des plantes. Les endophytes racinaires sont ubiquistes. Ceux-ci incluent les endophytes foncés septés, dont on connaît mal le rôle dans la croissance des plantes et le maintien des communautés végétales. Dans cette revue, les auteurs ont pour objectifs d'évaluer les caractéristiques structurales des interactions entre les champignons endophytes foncés septés et les racines des angiospermes aussi bien que des gymnospermes, et de suggérer des avenues pour les recherches futures. L'étude en microscopie photonique des interactions endophyte-racine se retrouve dans plusieurs études qui montrent qu'une variété de caractéristiques structurales dépendent des espèces hôtes et des conditions de croissance. Dans certains cas, lorsque les hyphes pénètrent les racines, elles causent une rupture des cellules, alors que dans d'autres situations, il y a peu d'effet notable. Chez certaines espèces d'arbres, l'association avec ces endophytes peut ressembler à des ectomycorhizes ou à des ectendomycorhizes. Les rares études ultrastructurales indiquent que les hyphes intracellulaires ne possèdent pas d'enveloppe périfongique dérivée de l'hôte et de matériel matriciel interfacial, deux caractéristiques propres aux interactions cellulaires biotrophiques champignon-plante. Ceci soulève la question quant aux échanges entre ces champignons et les cellules végétales. D'autres recherches sur ces aspects sont nécessaires. On doit dé-velopper de nouvelles approches incluant la cytologie moléculaire et l'image...
Although roots of species in the Pinaceae are usually colonized by ectomycorrhizal (EM) fungi, there are increasing reports of the presence of arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi in these species. The objective of this study was to determine the colonization patterns in seedlings of three Pinus (pine) species (Pinus banksiana, Pinus strobus, Pinus contorta) and Picea glauca x Picea engelmannii (hybrid spruce) grown in soil collected from a disturbed forest site. Seedlings of all three pine species and hybrid spruce became colonized by EM, AM, and DSE fungi. The dominant EM morphotype belonged to the E-strain category; limited colonization by a Tuber sp. was found on roots of Pinus strobus and an unknown morphotype (cf. Suillus-Rhizopogon group) with thick, cottony white mycelium was present on short roots of all species. The three fungal categories tended to occupy different niches in a single root system. No correlation was found between the percent root colonized by EM and percent colonization by either AM or DSE, although there was a positive correlation between percent root length colonized by AM and DSE. Hyphae and vesicles were the only AM intracellular structures found in roots of all species; arbuscules were not observed in any roots.
Phyllotaxy describes the geometric arrangement of leaves and is important for plant productivity. Auxin is well known to regulate phyllotactic patterns via PIN1-dependent auxin polar transport, and studies of maize (Zea mays) aberrant phyllotaxy1 (abph1) mutants suggest the importance of auxin and cytokinin signaling for control of phyllotaxy. However, whether additional regulators control these patterns is poorly understood. Here, we report a new dominant maize mutant, Aberrant phyllotaxy2 (Abph2), in which the shoot meristems are enlarged and the phyllotactic pattern switches from alternate to decussate. Map-based cloning revealed that the Abph2 mutation was caused by transposition of a glutaredoxin gene, MALE STERILE CONVERTED ANTHER1 (MSCA1), which gained an altered expression pattern in Abph2 mutant embryos. msca1 loss-of-function mutants have reduced meristem size and revealed a novel function of glutaredoxins in meristem growth. In addition, MSCA1 interacts with a TGA transcription factor, FASCIATED EAR4, suggesting a novel regulatory module for regulating shoot meristem size.
Tomato (Solanum lycopersicum) produces a wide range of volatile chemicals during fruit ripening, generating a distinct aroma and contributing to the overall flavor. Among these volatiles are several aromatic and aliphatic nitrogen-containing compounds for which the biosynthetic pathways are not known. While nitrogenous volatiles are abundant in tomato fruit, their content in fruits of the closely related species of the tomato clade is highly variable. For example, the green-fruited species Solanum pennellii are nearly devoid, while the red-fruited species S. lycopersicum and Solanum pimpinellifolium accumulate high amounts. Using an introgression population derived from S. pennellii, we identified a locus essential for the production of all the detectable nitrogenous volatiles in tomato fruit. Silencing of the underlying gene (SlTNH1;Solyc12g013690) in transgenic plants abolished production of aliphatic and aromatic nitrogenous volatiles in ripe fruit, and metabolomic analysis of these fruit revealed the accumulation of 2-isobutyl-tetrahydrothiazolidine-4-carboxylic acid, a known conjugate of cysteine and 3-methylbutanal. Biosynthetic incorporation of stable isotope-labeled precursors into 2-isobutylthiazole and 2-phenylacetonitrile confirmed that cysteine provides the nitrogen atom for all nitrogenous volatiles in tomato fruit. Nicotiana benthamiana plants expressing SlTNH1 readily transformed synthetic 2-substituted tetrahydrothiazolidine-4-carboxylic acid substrates into a mixture of the corresponding 2-substituted oxime, nitro, and nitrile volatiles. Distinct from other known flavin-dependent monooxygenase enzymes in plants, this tetrahydrothiazolidine-4-carboxylic acid N-hydroxylase catalyzes sequential hydroxylations. Elucidation of this pathway is a major step forward in understanding and ultimately improving tomato flavor quality.
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