YUCCA-Mediated Biosynthesis of the Auxin IAA Is Required during the Somatic Embryogenic Induction Process in Coffea canephora

Uc-Chuc, Miguel A.; Pérez-Hernández, Cleyre; Galáz-Ávalos, Rosa M.; Brito‐Argáez, Ligia; Aguilar-Hernández, Víctor; Loyola‐Vargas, Víctor M.

doi:10.3390/ijms21134751

Cited by 16 publications

(21 citation statements)

References 81 publications

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“…In this system, the quadruple yuc1 yuc2 yuc4 yuc6 mutant shows a normal progression of somatic embryogenesis, while the yuc1 yuc4 yuc10 yuc11 mutant produces only a few malformed somatic embryos ( Bai et al, 2013 ). Treatment with the YUC enzyme inhibitor yucasin drastically reduces somatic embryo formation from Coffea canephora explants ( Uc-Chuc et al, 2020 ). It is clear that endogenous auxin biosynthesis has a role in 2,4-D-induced somatic embryo induction, but when and how auxin biosynthesis specifically promotes somatic embryogenesis is not known.…”

Section: Introductionmentioning

confidence: 99%

Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis

Wróbel-Marek

Heidmann

et al. 2021

Plant Physiology

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Somatic embryogenesis is a type of plant cell totipotency where embryos develop from non-reproductive (vegetative) cells without fertilization. Somatic embryogenesis can be induced in vitro by auxins, and by ectopic expression of embryo-expressed transcription factors like the BABY BOOM (BBM) AINTEGUMENTA-LIKE APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) domain protein. These different pathways are thought to converge to promote auxin response and biosynthesis, but the specific roles of the endogenous auxin pathway in somatic embryogenesis induction have not been well-characterized. Here we show that BBM transcriptionally regulates the YUCCA3 (YUC3) and YUC8 auxin biosynthesis genes during BBM-mediated somatic embryogenesis in Arabidopsis (Arabidopsis thaliana) seedlings. BBM induced local and ectopic YUC3 and YUC8 expression in seedlings, which coincided with increased DR5 auxin response and indole-3-acetic acid (IAA) biosynthesis and with ectopic expression of the WOX2 embryo reporter. YUC-driven auxin biosynthesis was required for BBM-mediated somatic embryogenesis, as the number of embryogenic explants was reduced by ca. 50% in yuc3 yuc8 mutants and abolished after chemical inhibition of YUC enzyme activity. However, a detailed YUC inhibitor time-course study revealed that YUC-dependent IAA biosynthesis is not required for the re-initiation of totipotent cell identity in seedlings. Rather, YUC enzymes are required later in somatic embryo development for the maintenance of embryo identity and growth. This study resolves a long-standing question about the role of endogenous auxin biosynthesis in transcription factor-mediated somatic embryogenesis and also provides an experimental framework for understanding the role of endogenous auxin biosynthesis in other in planta and in vitro embryogenesis systems.

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Section: Introductionmentioning

confidence: 99%

Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis

Wróbel-Marek

Heidmann

et al. 2021

Plant Physiology

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“…For example, during the SE of C. canephora , the addition of exogenous auxin induces endogenous IAA accumulation [ 28 ]. This increase in the IAA level during pretreatment is due to de novo biosynthesis [ 29 ]. Currently, no gene related to the conjugation of IAA with amino acids has been characterized in C. canephora .…”

Section: Discussionmentioning

confidence: 99%

“…Auxin controls different cellular processes, including the induction of somatic embryogenesis, so its levels must be precisely regulated. Auxin homeostasis can be regulated in various ways, and endogenous levels can be altered by its conjugation [ 29 , 61 ]. There is increasing evidence that conjugation reactions through GH3 play an important role in these regulatory processes [ 24 ], in particular, the inactivation of IAA through conjugation with amino acids [ 16 ].…”

Section: Discussionmentioning

confidence: 99%

“…For example, in carrot cell cultures, it was observed that the use of 2,4-dichlorophenoxyacetic acid in the culture medium stimulates the accumulation of endogenous IAA and amide conjugates [ 27 ]. During the induction of SE in Coffea canephora , it was determined that the addition of an exogenous auxin during pretreatment of the source of the explants produces a sharp increase in the content of free IAA and some of its conjugates, such as IAA–Glu and IAA–Ala [ 28 , 29 ]. These results suggest that endogenous IAA accumulation appears to be essential for the changing of a cell’s fate before the beginning of the embryogenic pathway.…”

Section: Introductionmentioning

confidence: 99%

“…In our laboratory, we have developed an efficient system for obtaining somatic embryos from foliar explants of C. canephora [ 37 ]. We have used this system to study diverse aspects of the induction of SE [ 29 , 38 , 39 , 40 , 41 ]. Recently, we elaborated a transcriptome of the induction of the SE in C. canephora [ 41 ].…”

Section: Introductionmentioning

confidence: 99%

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Genome-Wide Analysis, Modeling, and Identification of Amino Acid Binding Motifs Suggest the Involvement of GH3 Genes during Somatic Embryogenesis of Coffea canephora

Méndez-Hernández

Quintana-Escobar

Uc-Chuc

et al. 2021

Plants

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Auxin plays a central role in growth and plant development. To maintain auxin homeostasis, biological processes such as biosynthesis, transport, degradation, and reversible conjugation are essential. The Gretchen Hagen 3 (GH3) family genes codify for the enzymes that esterify indole-3-acetic acid (IAA) to various amino acids, which is a key process in the induction of somatic embryogenesis (SE). The GH3 family is one of the principal families of early response to auxin genes, exhibiting IAA-amido synthetase activity to maintain optimal levels of free auxin in the cell. In this study, we carried out a systematic identification of the GH3 gene family in the genome of Coffea canephora, determining a total of 18 CcGH3 genes. Analysis of the genetic structures and phylogenetic relationships of CcGH3 genes with GH3 genes from other plant species revealed that they could be clustered in two major categories with groups 1 and 2 of the GH3 family of Arabidopsis. We analyzed the transcriptome expression profiles of the 18 CcGH3 genes using RNA-Seq analysis-based data and qRT-PCR during the different points of somatic embryogenesis induction. Furthermore, the endogenous quantification of free and conjugated indole-3-acetic acid (IAA) suggests that the various members of the CcGH3 genes play a crucial role during the embryogenic process of C. canephora. Three-dimensional modeling of the selected CcGH3 proteins showed that they consist of two domains: an extensive N-terminal domain and a smaller C-terminal domain. All proteins analyzed in the present study shared a unique conserved structural topology. Additionally, we identified conserved regions that could function to bind nucleotides and specific amino acids for the conjugation of IAA during SE in C. canephora. These results provide a better understanding of the C. canephora GH3 gene family for further exploration and possible genetic manipulation.

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Identification, analysis, and modeling of the YUCCA protein family genome‐wide in Coffea canephora

2021

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Auxin is involved in almost every aspect of plant growth and development, from embryogenesis to senescence. Indole-3-acetic acid (IAA) is the main known natural auxin that is synthesized by enzymes tryptophan aminotransferase of arabidopsis (TAA) and YUCCA (YUC) of the flavin-containing monooxygenases family (FMO) from one of the tryptophan-dependent pathways. Genome-wide identification and comprehensive analysis of the YUC-protein family have been conducted in Coffea canephora in the present study. A total of 10 members CcYUC gene family were identified in C. canephora. Phylogenetic analysis revealed that the CcYUC protein family is evolutionarily conserved, and they consist of four groups. In contrast, bioinformatic analysis predicted a hydrophobic transmembrane helix (TMH) for one CcYUC (YUC10) member only. Isoelectric point (pI), molecular mass (Ms), signal peptide, subcellular localization, and phosphorylation sites were predicted for CcYUC proteins.YUC enzymes require the prosthetic group flavin adenine dinucleotide (FAD) and the cofactor nicotinamide adenine dinucleotide phosphate (NADPH) for their enzymatic activity. Therefore, we include the molecular docking for CcYUC2-FAD-NADPH-IPyA and yucasin, which is a specific inhibitor for YUC activity. The docking results showed FAD and NADPH binding at the big and small domain sites, respectively, in CcYUC2. IPyA binds very close to FAD along the big domain, and yucasin competes for the same site as IPA, blocking IAA production. Furthermore, in silico point mutations affect the stability of the CcYUC2-4 proteins.

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YUCCA-Mediated Biosynthesis of the Auxin IAA Is Required during the Somatic Embryogenic Induction Process in Coffea canephora

Cited by 16 publications

References 81 publications

Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis

Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis

Genome-Wide Analysis, Modeling, and Identification of Amino Acid Binding Motifs Suggest the Involvement of GH3 Genes during Somatic Embryogenesis of Coffea canephora

Identification, analysis, and modeling of the YUCCA protein family genome‐wide in Coffea canephora

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