The function of the RNA-binding protein TEL1 in moss reveals ancient regulatory mechanisms of shoot development

Abstract

The shoot represents the basic body plan in land plants. It consists of a repeated structure composed of stems and leaves. Whereas vascular plants generate a shoot in their diploid phase, non-vascular plants such as mosses form a shoot (called the gametophore) in their haploid generation. The evolution of regulatory mechanisms or genetic networks used in the development of these two kinds of shoots is unclear. TERMINAL EAR1-like genes have been involved in diploid shoot development in vascular plants. Here, we show that disruption of PpTEL1 from the moss Physcomitrella patens, causes reduced protonema growth and gametophore initiation, as well as defects in gametophore development. Leafy shoots formed on ΔTEL1 mutants exhibit shorter stems with more leaves per shoot, suggesting an accelerated leaf initiation (shortened plastochron), a phenotype shared with the Poaceae vascular plants TE1 and PLA2/LHD2 mutants. Moreover, the positive correlation between plastochron length and leaf size observed in ΔTEL1 mutants suggests a conserved compensatory mechanism correlating leaf growth and leaf initiation rate that would minimize overall changes in plant biomass. The RNA-binding protein encoded by PpTEL1 contains two N-terminus RNA-recognition motifs, and a third C-terminus non-canonical RRM, specific to TEL proteins. Removal of the PpTEL1 C-terminus (including this third RRM) or only 16-18 amino acids within it seriously impairs PpTEL1 function, suggesting a critical role for this third RRM. These results show a conserved function of the RNA-binding PpTEL1 protein in the regulation of shoot development, from early ancestors to vascular plants, that depends on the third TEL-specific RRM.

Plant evolution at the interface of paleontology and developmental biology: An organism‐centered paradigm

“…24, 25). Along with P. patens sporophytes that produce multiple sporangia as a result of disruption of different genetic loci or inhibition of polar auxin transport (Tanahashi et al, 2005; Fujita et al, 2008; Vivancos et al, 2012), these findings corroborate developmental anatomy and teratological observations and point to putative mechanisms for acquisition of growth indeterminacy and modularity.…”

Transcriptome analysis during berry development provides insights into co-regulated and altered gene expression between a seeded wine grape variety and its seedless somatic variant

“…Among the genes involved in cellular processes we selected TERMINAL EAR1- like 1 ( TEL1 , VIT_14s0219g00270) and Fimbrin 2 (VIT_12s0059g00560). The TEL1 gene encodes an RNA binding protein with a function in shoot development, conserved among land and vascular plants [ 51 , 82 ]. The Arabidopsis best match of TEL1 is a member of the MEI2 -like gene family, which plays a role in meiosis.…”

The origin and early evolution of vascular plant shoots and leaves

“…There are no PpLFY gain-of-function mutants and the downstream targets of PpLFY are not yet known, so it is hard to interpret the Physcomitrella Pplfy mutant phenotype in light of the evolution of branching. Similarly the low penetrance branching mutant phenotype of Pptel mutants is hard to interpret because TEL encodes an RNA binding protein, and the specificity of PpTEL action is not known [ 71 ]. The cellular and developmental basis of branching in the mutants above remains an open question, but the low penetrance of branching phenotypes suggests that an element of stochasticity is involved in the development of moss sporophyte branching, potentially in early embryonic cell fate specification.…”