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The dynamics of soybean leaf and shoot apical meristem transcriptome undergoing floral initiation process.

Wong CE, Singh MB, Bhalla PL - PLoS ONE (2013)

Bottom Line: A total of 2951 shoot apical meristem and 13,609 leaf sequences with significant profile changes during the time course examined were identified.Transcripts associated with protein degradation were also significantly changing in leaf and SAM implicating their involvement in triggering the developmental switch.Further, evidence is emerging that the conversion of shoot apical meristem to inflorescence meristem is linked with the interplay of auxin, cytokinin and GA creating a low cytokinin and high GA environment.

View Article: PubMed Central - PubMed

Affiliation: Plant Molecular Biology and Biotechnology Group, ARC Centre of Excellence for Integrative Legume Research, Melbourne School of Land and Environment, The University of Melbourne, Parkville, Victoria, Australia.

ABSTRACT
Flowering process governs seed set and thus affects agricultural productivity. Soybean, a major legume crop, requires short-day photoperiod conditions for flowering. While leaf-derived signal(s) are essential for the photoperiod-induced floral initiation process at the shoot apical meristem, molecular events associated with early floral transition stages in either leaves or shoot apical meristems are not well understood. To provide novel insights into the molecular basis of floral initiation, RNA-Seq was used to characterize the soybean transcriptome of leaf and micro-dissected shoot apical meristem at different time points after short-day treatment. Shoot apical meristem expressed a higher number of transcripts in comparison to that of leaf highlighting greater diversity and abundance of transcripts expressed in the shoot apical meristem. A total of 2951 shoot apical meristem and 13,609 leaf sequences with significant profile changes during the time course examined were identified. Most changes in mRNA level occurred after 1short-day treatment. Transcripts involved in mediating responses to stimulus including hormones or in various metabolic processes represent the top enriched GO functional category for the SAM and leaf dataset, respectively. Transcripts associated with protein degradation were also significantly changing in leaf and SAM implicating their involvement in triggering the developmental switch. RNA-Seq analysis of shoot apical meristem and leaf from soybean undergoing floral transition reveal major reprogramming events in leaves and the SAM that point toward hormones gibberellins (GA) and cytokinin as key regulators in the production of systemic flowering signal(s) in leaves. These hormones may form part of the systemic signals in addition to the established florigen, FLOWERING LOCUS T (FT). Further, evidence is emerging that the conversion of shoot apical meristem to inflorescence meristem is linked with the interplay of auxin, cytokinin and GA creating a low cytokinin and high GA environment.

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Related in: MedlinePlus

Expression of putative cytokinin biosynthesis and signaling genes in soybean.The rate-limiting step of cytokinin biosynthesis is catalyzed by ATP/ADP-ISOPENTENYLTRASNFERASE (IPT) gene family as indicated by the schematic diagram [60] on the left. Transmembrane histidine kinases (HK3, HK4) are cytokinin receptors that are auto-phosphorylated following the initial cytokinin perception. These then transfer the phosphate group to members of the HISTIDINE PHOSPHOTRANSFER proteins (HP1, 4, 6) family. HPs subsequently translocate to the nucleus to phosphorylate the RESPONSE REGULATORs (ARRs) proteins of either type-A or type-B. Activated type-A and type-B RRs negatively and positively regulate cytokinin signaling, respectively. Expression level is as in Figure 3.
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pone-0065319-g007: Expression of putative cytokinin biosynthesis and signaling genes in soybean.The rate-limiting step of cytokinin biosynthesis is catalyzed by ATP/ADP-ISOPENTENYLTRASNFERASE (IPT) gene family as indicated by the schematic diagram [60] on the left. Transmembrane histidine kinases (HK3, HK4) are cytokinin receptors that are auto-phosphorylated following the initial cytokinin perception. These then transfer the phosphate group to members of the HISTIDINE PHOSPHOTRANSFER proteins (HP1, 4, 6) family. HPs subsequently translocate to the nucleus to phosphorylate the RESPONSE REGULATORs (ARRs) proteins of either type-A or type-B. Activated type-A and type-B RRs negatively and positively regulate cytokinin signaling, respectively. Expression level is as in Figure 3.

Mentions: There is an overall increase of transcripts related to cytokinin biosynthesis and signaling that can be interpreted as an increase in the hormone level in the leaf following 1short-day (Figure 7). Sequences annotated as CYTOKININ OXIDASE (Glyma12g01390.1, Glyma11g20860.1, Glyma09g35950.1, Glyma04g05840.1) that degrades cytokinin were also significantly up-regulated suggesting there is a likely attenuation or enhancement of cytokinin signaling depending on the cell type. The possible increase of cytokinin level in the leaf may precede the induction of floral meristem identity genes in the SAM. An increased level of cytokinin has been found first in the leaf extracts followed by the SAM of Arabidopsis plants induced to flower by a single long-day and the application of cytokinin has also been found to promote flowering in Arabidopsis under short-days [58], [59]. It is therefore tempting to speculate that the initial heightened cytokinin-mediated signaling is to orchestrate the network necessary to bring about the transport of flowering signals including cytokinin to the SAM. Furthermore, while there was no significant up-regulation of cytokinin biosynthesis gene in the SAM (Figure 7), there was an up-regulation of several cytokinin signaling components suggesting a possible contribution of leaf-derived cytokinin to the increase of cytokinin level in the SAM leading to the up-regulation of these sequences. The cytokinin signaling components activated in the SAM that are of particular interest include a putative HISTIDINE PHOSPHOTRANSFER PROTEIN 6 (HP6) homeolog pair and B-type response regulators (RR12, Glyma13g22320.1; RR18, Glyma17g08380.1) that are positive regulators in the cytokinin signaling circuitry. While GmHP6s (Glyma08g22720.1, Glyma07g03390.1) show exclusive expression in the SAM with an increased expression on 1-short-day that peaked at 2-short-day and subsequently down-regulated, GmRR12 and GmRR18 showed similar expression dynamics to that of GmSOC1 with at least 3-fold induction in the SAM on 3-short-day indicating they can be novel regulator in the SAM during the floral initiation process (Figures 3 & 7). As HPs are proposed to mediate signaling between the plasma membrane–bound cytokinin receptors and the response regulators within the nucleus [60], the timing of the up-regulation of GmHP6 followed by GmRR12 and GmRR18 implicates GmHP6 likely act upstream of these response regulators.


The dynamics of soybean leaf and shoot apical meristem transcriptome undergoing floral initiation process.

Wong CE, Singh MB, Bhalla PL - PLoS ONE (2013)

Expression of putative cytokinin biosynthesis and signaling genes in soybean.The rate-limiting step of cytokinin biosynthesis is catalyzed by ATP/ADP-ISOPENTENYLTRASNFERASE (IPT) gene family as indicated by the schematic diagram [60] on the left. Transmembrane histidine kinases (HK3, HK4) are cytokinin receptors that are auto-phosphorylated following the initial cytokinin perception. These then transfer the phosphate group to members of the HISTIDINE PHOSPHOTRANSFER proteins (HP1, 4, 6) family. HPs subsequently translocate to the nucleus to phosphorylate the RESPONSE REGULATORs (ARRs) proteins of either type-A or type-B. Activated type-A and type-B RRs negatively and positively regulate cytokinin signaling, respectively. Expression level is as in Figure 3.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3675103&req=5

pone-0065319-g007: Expression of putative cytokinin biosynthesis and signaling genes in soybean.The rate-limiting step of cytokinin biosynthesis is catalyzed by ATP/ADP-ISOPENTENYLTRASNFERASE (IPT) gene family as indicated by the schematic diagram [60] on the left. Transmembrane histidine kinases (HK3, HK4) are cytokinin receptors that are auto-phosphorylated following the initial cytokinin perception. These then transfer the phosphate group to members of the HISTIDINE PHOSPHOTRANSFER proteins (HP1, 4, 6) family. HPs subsequently translocate to the nucleus to phosphorylate the RESPONSE REGULATORs (ARRs) proteins of either type-A or type-B. Activated type-A and type-B RRs negatively and positively regulate cytokinin signaling, respectively. Expression level is as in Figure 3.
Mentions: There is an overall increase of transcripts related to cytokinin biosynthesis and signaling that can be interpreted as an increase in the hormone level in the leaf following 1short-day (Figure 7). Sequences annotated as CYTOKININ OXIDASE (Glyma12g01390.1, Glyma11g20860.1, Glyma09g35950.1, Glyma04g05840.1) that degrades cytokinin were also significantly up-regulated suggesting there is a likely attenuation or enhancement of cytokinin signaling depending on the cell type. The possible increase of cytokinin level in the leaf may precede the induction of floral meristem identity genes in the SAM. An increased level of cytokinin has been found first in the leaf extracts followed by the SAM of Arabidopsis plants induced to flower by a single long-day and the application of cytokinin has also been found to promote flowering in Arabidopsis under short-days [58], [59]. It is therefore tempting to speculate that the initial heightened cytokinin-mediated signaling is to orchestrate the network necessary to bring about the transport of flowering signals including cytokinin to the SAM. Furthermore, while there was no significant up-regulation of cytokinin biosynthesis gene in the SAM (Figure 7), there was an up-regulation of several cytokinin signaling components suggesting a possible contribution of leaf-derived cytokinin to the increase of cytokinin level in the SAM leading to the up-regulation of these sequences. The cytokinin signaling components activated in the SAM that are of particular interest include a putative HISTIDINE PHOSPHOTRANSFER PROTEIN 6 (HP6) homeolog pair and B-type response regulators (RR12, Glyma13g22320.1; RR18, Glyma17g08380.1) that are positive regulators in the cytokinin signaling circuitry. While GmHP6s (Glyma08g22720.1, Glyma07g03390.1) show exclusive expression in the SAM with an increased expression on 1-short-day that peaked at 2-short-day and subsequently down-regulated, GmRR12 and GmRR18 showed similar expression dynamics to that of GmSOC1 with at least 3-fold induction in the SAM on 3-short-day indicating they can be novel regulator in the SAM during the floral initiation process (Figures 3 & 7). As HPs are proposed to mediate signaling between the plasma membrane–bound cytokinin receptors and the response regulators within the nucleus [60], the timing of the up-regulation of GmHP6 followed by GmRR12 and GmRR18 implicates GmHP6 likely act upstream of these response regulators.

Bottom Line: A total of 2951 shoot apical meristem and 13,609 leaf sequences with significant profile changes during the time course examined were identified.Transcripts associated with protein degradation were also significantly changing in leaf and SAM implicating their involvement in triggering the developmental switch.Further, evidence is emerging that the conversion of shoot apical meristem to inflorescence meristem is linked with the interplay of auxin, cytokinin and GA creating a low cytokinin and high GA environment.

View Article: PubMed Central - PubMed

Affiliation: Plant Molecular Biology and Biotechnology Group, ARC Centre of Excellence for Integrative Legume Research, Melbourne School of Land and Environment, The University of Melbourne, Parkville, Victoria, Australia.

ABSTRACT
Flowering process governs seed set and thus affects agricultural productivity. Soybean, a major legume crop, requires short-day photoperiod conditions for flowering. While leaf-derived signal(s) are essential for the photoperiod-induced floral initiation process at the shoot apical meristem, molecular events associated with early floral transition stages in either leaves or shoot apical meristems are not well understood. To provide novel insights into the molecular basis of floral initiation, RNA-Seq was used to characterize the soybean transcriptome of leaf and micro-dissected shoot apical meristem at different time points after short-day treatment. Shoot apical meristem expressed a higher number of transcripts in comparison to that of leaf highlighting greater diversity and abundance of transcripts expressed in the shoot apical meristem. A total of 2951 shoot apical meristem and 13,609 leaf sequences with significant profile changes during the time course examined were identified. Most changes in mRNA level occurred after 1short-day treatment. Transcripts involved in mediating responses to stimulus including hormones or in various metabolic processes represent the top enriched GO functional category for the SAM and leaf dataset, respectively. Transcripts associated with protein degradation were also significantly changing in leaf and SAM implicating their involvement in triggering the developmental switch. RNA-Seq analysis of shoot apical meristem and leaf from soybean undergoing floral transition reveal major reprogramming events in leaves and the SAM that point toward hormones gibberellins (GA) and cytokinin as key regulators in the production of systemic flowering signal(s) in leaves. These hormones may form part of the systemic signals in addition to the established florigen, FLOWERING LOCUS T (FT). Further, evidence is emerging that the conversion of shoot apical meristem to inflorescence meristem is linked with the interplay of auxin, cytokinin and GA creating a low cytokinin and high GA environment.

Show MeSH
Related in: MedlinePlus