Transcriptomics insights into the genetic regulation of root apical meristem exhaustion and determinate primary root growth in Pachycereus pringlei (Cactaceae)

Abstract

Many Cactaceae species exhibit determinate growth of the primary root as a consequence of root apical meristem (RAM) exhaustion. The genetic regulation of this growth pattern is unknown. Here, we de novo assembled and annotated the root apex transcriptome of the Pachycereus pringlei primary root at three developmental stages, with active or exhausted RAM. The assembled transcriptome is robust and comprehensive, and was used to infer a transcriptional regulatory network of the primary root apex. Putative orthologues of Arabidopsis regulators of RAM maintenance, as well as putative lineage-specific transcripts were identified. The transcriptome revealed putative orthologues of most proteins involved in housekeeping processes, hormone signalling, and metabolic pathways. Our results suggest that specific transcriptional programs operate in the root apex at specific developmental time points. Moreover, the transcriptional state of the P. pringlei root apex as the RAM becomes exhausted is comparable to the transcriptional state of cells from the meristematic, elongation, and differentiation zones of Arabidopsis roots along the root axis. We suggest that the transcriptional program underlying the drought stress response is induced during Cactaceae root development, and that lineage-specific transcripts could contribute to RAM exhaustion in Cactaceae.

Development and cell cycle dynamics of the root apical meristem in the fernCeratopteris richardii

“…The termination of root growth suggests that Ceratopteris SBRs follow a determinate growth program, even in the presence of nutritional sufficiency. This is concordant with the concept of primary homorhizy indicating that, at least, the first SBR has a short time span (Schneider, 2013 terminal stage displayed a similar transcriptional profile to the differentiation zone of Arabidopsis, where genes involved stemness and proliferation are downregulated (Benesova, 2016;Gutierrez-Alanis et al, 2015;Rodriguez-Alonso et al, 2018;Rodriguez-Rodriguez et al, 2003).…”

Modulatory Role of Reactive Oxygen Species in Root Development in Model Plant of Arabidopsis thaliana

“…Root growth relies on the balance of proliferation and differentiation in root stem cells (Petricka et al, 2012). Plant root systems can be divided into three zones along the longitudinal axis; namely, the meristematic, elongation, and maturation zones (Rodriguez-Alonso et al, 2018). The most characteristic stem cells of plants are in the shoot apical meristem and root apical meristem (Sarkar et al, 2007).…”

Rooting in the Desert: A Developmental Overview on Desert Plants

“…This positions mature xylem cells closer to the root tip, allowing rapid water uptake during spontaneous rainfall [34]. Transcriptome analysis of active and differentiated meristems of roots of the cactus Pachycereus pringlei identified orthologues of Arabidopsis developmental regulators, such as the GRAS-domain transcription cofactors SHR and SCR, as well as the transcription factor JKD, which regulate ground tissue and QC specification in Arabidopsis [35,36]. This study also revealed an upregulation of genes involved in abscisic acid (ABA) responses at the determinate stage [35].…”

“…Transcriptome analysis of active and differentiated meristems of roots of the cactus Pachycereus pringlei identified orthologues of Arabidopsis developmental regulators, such as the GRAS-domain transcription cofactors SHR and SCR, as well as the transcription factor JKD, which regulate ground tissue and QC specification in Arabidopsis [35,36]. This study also revealed an upregulation of genes involved in abscisic acid (ABA) responses at the determinate stage [35]. With the role of ABA in mediating the response to drought, it is plausible that cactus tolerance to drought might be mediated by an increase in ABA levels, while meristem differentiation might result from a change in hormone homeostasis and an alteration of stem cell regulatory networks.…”

“…Analysis of the root apex transcriptome of Pachycereus pringlei, showed that orthologues of most genes associated with auxin and cytokinin signaling pathways are present in the transcriptome. Differentially upregulated transcripts in the terminal developmental stage include transcripts for proteins involved in auxin-related processes, such as AUXIN RESPONSE FACTORs and SMALL AUXIN UP RNAs [35]. It would be also informative to determine whether the stem cell loss involves the jasmonic acid regulatory module, similar to Arabidopsis [43].…”