TL;DR: It is shown that lateral leaflet formation in C. hirsuta requires the establishment of growth foci that form after leaf initiation, and evidence is provided that differential deployment of a fundamental mechanism polarizing cellular growth contributed to the diversification of leaf form during evolution.
Abstract: The developmental basis for the generation of divergent leaf forms is largely unknown. Here we investigate this problem by studying processes that distinguish development of two related species: Arabidopsis thaliana, which has simple leaves, and Cardamine hirsuta, which has dissected leaves with individual leaflets. Using genetics, expression studies and cell lineage tracing, we show that lateral leaflet formation in C. hirsuta requires the establishment of growth foci that form after leaf initiation. These growth foci are recruited at the leaf margin in response to activity maxima of auxin, a hormone that polarizes growth in diverse developmental contexts. Class I KNOTTED1-like homeobox (KNOX) proteins also promote leaflet initiation in C. hirsuta, and here we provide evidence that this action of KNOX proteins is contingent on the ability to organize auxin maxima via the PINFORMED1 (PIN1) auxin efflux transporter. Thus, differential deployment of a fundamental mechanism polarizing cellular growth contributed to the diversification of leaf form during evolution.
TL;DR: The results show that GOB marks leaflet boundaries and that its accurate spatial, temporal and quantitative activity affects leaf elaboration in a context-dependent manner.
Abstract: Leaves are formed at the flanks of the shoot apical meristem (SAM) and develop into a variety of forms. In tomato, prolonged leaf patterning enables the elaboration of compound leaves by reiterative initiation of leaflets with lobed margins. In goblet (gob) loss-of-function mutants, primary leaflets are often fused, secondary leaflets and marginal serrations are absent, and SAMs often terminate precociously. We show that GOB encodes a NAC-domain transcription factor expressed in narrow stripes at the leaf margins, flanking the distal side of future leaflet primordia, and at the boundaries between the SAM and leaf primordia. Leaf-specific overexpression of the microRNA miR164, a negative regulator of GOB-like genes, also leads to loss of secondary-leaflet initiation and to smooth leaflet margins. Plants carrying a dominant gob allele with an intact ORF but disrupted miR164 binding site produce more cotyledons and floral organs, have split SAMs and, surprisingly, simpler leaves. Overexpression of a form of GOB with an altered miR164 binding site in leaf primordia leads to delayed leaflet maturation, frequent, improperly timed and spaced initiation events, and a simple mature leaflet form owing to secondary-leaflet fusion. miR164 also affects leaflet separation in Cardamine hirsuta, a Brassicaceae species with complex leaves. Genetic and molecular analyses suggest that GOB expression is intact in the simplified leaves of entire tomato mutants, which have a defect in a putative repressor of auxin responses. Our results show that GOB marks leaflet boundaries and that its accurate spatial, temporal and quantitative activity affects leaf elaboration in a context-dependent manner.
TL;DR: This is the first demonstration of exploitation competition for plant assimilates between two insect—induced sinks, mediated by manipulation of plant phloem transport, stands in contrast to the absence of interference competition for galling sites between the two aphid species.
Abstract: The role of interspecific interactions among herbivorous insects is considered to be limited, especially in specialist communities. In the current study we report on exploitative interspecific interaction between two closely related phloem—feeding species of gall—forming aphids (Homoptera; Pemphigidae; Fordinae), mediated by the supply of photoassimilates from the host plant. Geoica sp. forms a spherical gall on the leaflet midrib of Pistacia palaestina (Anacardiaceae), while Forda formicaria forms crescent—shaped galls on the leaflet margin of the same host plant. Using 14C labeling, we were able to trace the food supply (assimilated carbohydrates) from the leaves to galls of each species. We found that Geoica galls are strong sinks. These galls divert the normal phloem transport of the plant and reduce the amount of assimilates imported by F. formicaria, especially when they are located on the same leaflet. By the end of the season Geoica caused death of 84% of F. formicaria galls that were located on the same leaflet, and reduced reproductive success in the surviving galls by 20%. This is because the presence of Geoica causes early senescence (but not abscission) of the leaflet it is on (whether or not F. formicaria is present). The interaction is asymmetrical: F. formicaria did not affect reproductive output of Geoica nor did it cause visible damage to the leaflets. To our knowledge, this it the first demonstration of exploitation competition for plant assimilates between two insect—induced sinks. This exploitative competition, mediated by manipulation of plant phloem transport, stands in contrast to the absence of interference competition for galling sites between the two aphid species. Although their spatial distributions partly overlapped, the niche breadth of each species (measured from gall positions on leaves along the shoot axis) was not affected by the presence of the other. Moreover, when both species were located on the same leaf, they formed galls independently on the same or different leaflets, and there was no indication of interference competition over galling sites.
TL;DR: It is shown that UNI is expressed in the leaf blastozone over the period in which organ primordia are initiated and is downregulated at the time of leaf primordium determination, and proposed that the control of UNI expression by AF, TL, and COCH is important in the regulation of Blastozone activity and pattern formation in the compound leafPrimordium of the pea.
Abstract: The compound leaf primordium of pea represents a marginal blastozone that initiates organ primordia, in an acropetal manner, from its growing distal region. The UNIFOLIATA (UNI) gene is important in marginal blastozone maintenance because loss or reduction of its function results in uni mutant leaves of reduced complexity. In this study, we show that UNI is expressed in the leaf blastozone over the period in which organ primordia are initiated and is downregulated at the time of leaf primordium determination. Prolonged UNI expression was associated with increased blastozone activity in the complex leaves of afila (af), cochleata (coch), and afila tendril-less (af tl) mutant plants. Our analysis suggests that UNI expression is negatively regulated by COCH in stipule primordia, by AF in proximal leaflet primordia, and by AF and TL in distal and terminal tendril primordia. We propose that the control of UNI expression by AF, TL, and COCH is important in the regulation of blastozone activity and pattern formation in the compound leaf primordium of the pea.