Genome-Wide Analyses of MADS-Box Genes in Humulus lupulus L. Reveal Potential Participation in Plant Development, Floral Architecture, and Lupulin Gland Metabolism

Abstract

MADS-box transcription factors (TFs) are involved in multiple plant development processes and are most known during the reproductive transition and floral organ development. Very few genes have been characterized in the genome of Humulus lupulus L. (Cannabaceae), an important crop for the pharmaceutical and beverage industries. The MADS-box family has not been studied in this species yet. We identified 65 MADS-box genes in the hop genome, of which 29 encode type-II TFs (27 of subgroup MIKCC and 2 MIKC*) and 36 type-I proteins (26 α, 9 β, and 1 γ). Type-II MADS-box genes evolved more complex architectures than type-I genes. Interestingly, we did not find FLOWERING LOCUS C (FLC) homologs, a transcription factor that acts as a floral repressor and is negatively regulated by cold. This result provides a molecular explanation for a previous work showing that vernalization is not a requirement for hop flowering, which has implications for its cultivation in the tropics. Analysis of gene ontology and expression profiling revealed genes potentially involved in the development of male and female floral structures based on the differential expression of ABC homeotic genes in each whorl of the flower. We identified a gene exclusively expressed in lupulin glands, suggesting a role in specialized metabolism in these structures. In toto, this work contributes to understanding the evolutionary history of MADS-box genes in hop, and provides perspectives on functional genetic studies, biotechnology, and crop breeding.

Genome-wide identification and expression analysis of MADS-box transcription factors reveal their involvement in sex determination of hardy rubber tree (Eucommia ulmoides oliv.)

“…Gray ex Hook (105 genes) ( Leseberg et al, 2006 ). Interestingly, the size of MADS-box TF family identified in H. lupulus (65) ( Gutierrez et al, 2022 ) is very close to the numbers of EuMADS TFs we found here. Neither male nor female flowers in E. ulmoides comprise sepal and petal, only have bracts encompassing 8–12 stamens (male) or one pistil (female) ( Wang et al, 2020 ).…”

“…The MADS-box TF family has been studied in certain species with bisexual flowers, e.g., tomato (137 genes) ( Wang et al, 2019 ), foxtail millet (89 genes) ( Lai et al, 2022 ) and American beautyberry (78 genes) ( Alhindi and Al-Abdallat, 2021 ), and a few species with unisexual flowers, such as litchi ( L. chinensis , 101 genes) ( Guan et al, 2021 ), hop ( H. lupulus L., 65 genes) ( Gutierrez et al, 2022 ) and Populus trichocarpa Torr. & A.…”

“…M-type subfamily generally contains SRF domain and is classified into three lineages, i.e., Mα, Mβ, and Mγ ( Wang et al, 2019 ). Whereas, MIKC subfamily usually possesses SRF or MEF2 domains and is divided into two lineages: MIKC * and MIKC C (superscript C means classic) ( Gutierrez et al, 2022 ). Wherein genes belong to MIKC C are the most well-studied MADS-box genes by far, they contain as many as 13 subgroups: AG/SHP, AGL6, AGL12, AGL15, ANR1, AP1, AP3/PI, FLC, SEP, SOC1, SVP, TM8, and TT16 ( Theißen et al, 2016 ; Alhindi and Al-Abdallat, 2021 ).…”

Mining the Roles of Cucumber DUF966 Genes in Fruit Development and Stress Response

“…The cucumber genome (ChineseLong_genome_v3) was downloaded from the CuGenDB ( , accessed on 18 June 2022). The hidden Markov model (HMM) of the DUF966 domain (PF06136) was downloaded from Pfam ( , accessed on 18 June 2022) and used as query sequences to perform first-round BLASTp against cucumber reference protein sequences (e-value < 10 −10 ) [ 33 ]. The reported DUF966 protein sequences were collected and used as query sequences to perform the second round of BLASTp [ 2 ].…”

Identification of MADS-Box Transcription Factors in Iris laevigata and Functional Assessment of IlSEP3 and IlSVP during Flowering

“…Nonetheless, all MADS-box proteins share the conserved MADS-box domain of around 60 amino acids in the N-terminus (also known as the M domain). Among them, MIKC-type genes encode plant-specific MADS-box proteins due to the presence of three additional domains (the intervening domain, keratin domain, and C-terminal domain) [ 17 ]. Two subtypes of MIKC, MIKC C , and MIKC*, have been recognized based on variances in the intervening domain [ 18 ].…”