Root growth is modulated by different factors, including phytohormones, transcription factors, and microRNAs (miRNAs). MicroRNA156 and its targets, the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes, define an age-dependent pathway that controls several developmental processes, including lateral root emergence. However, it remains unclear whether miR156-regulated SPLs control root meristem activity and root-derived de novo shoot regeneration. Here, we show that MIR156 and SPL genes have opposing expression patterns during the progression of primary root (PR) growth in Arabidopsis, suggesting that age cues may modulate root development. Plants with high miR156 levels display reduced meristem size, resulting in shorter primary root (PRs). Conversely, plants with reduced miR156 levels show higher meristem activity. Importantly, loss of function of SPL10 decreases meristem activity, while SPL10 de-repression increases it. Meristem activity is regulated by SPL10 probably through the reduction of cytokinin responses, via the modulation of type-B ARABIDOPSIS RESPONSE REGULATOR1(ARR1) expression. We also show that SPL10 de-repression in the PRs abolishes de novo shoot regenerative capacity by attenuating cytokinin responses. Our results reveal a cooperative regulation of root meristem activity and root-derived de novo shoot regeneration by integrating age cues with cytokinin responses via miR156-targeted SPL10.

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Fruits are originated from the transition of a quiescent ovary to a fast-growing young fruit. The evolution of reproductive structures such as ovary and fruit has made seed dispersal easier, which is a key process for reproductive success in flowering plants. The complete fruit development and ripening are characterized by a remarkable phenotypic plasticity which is orchestrated by a myriad of genetic factors. In this context, transcriptional regulation by non-coding small (i.e., microRNAs) and long (lncRNAs) RNAs underlies important mechanisms controlling reproductive organ development. These mechanisms may act together and interact with other pathways (i.e., phytohormones) to regulate cell fate and coordinate reproductive organ development. Functional genomics has shown that non-coding RNAs regulate a diversity of developmental reproductive stages, from carpel formation and ovary development to the softening of the ripe/ripened fruit. This layer of transcriptional control has been associated with ovule, seed, and fruit development as well as fruit ripening, which are crucial developmental processes in breeding programs because of their relevance for crop production. The final ripe fruit is the result of a process under multiple levels of regulation, including mechanisms orchestrated by microRNAs and lncRNAs. Most of the studies we discuss involve work on tomato and Arabidopsis. In this review, we summarize non-coding RNA-controlled mechanisms described in the current literature that act coordinating the main steps of gynoecium development/patterning and fruit ripening.

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