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Title:Female sterility and carpel development in plants
Author(s):Chakrabarty, Setu
Director of Research:Ming, Ray R
Doctoral Committee Chair(s):Ming, Ray R
Doctoral Committee Member(s):Zielinski, Raymond E; Tranel, Patrick J; Clough, Steven J
Department / Program:Plant Biology
Discipline:Plant Biology
Degree Granting Institution:University of Illinois at Urbana-Champaign
Subject(s):Arabidopsis, EMS, Carpel
Abstract:Angiosperms, or flowering plants, form the largest group of plants, with more than 350,000 extant species. They exhibit extensive diversity in shape, size, color, structure and organization of their reproductive organs contained within the flowers. With regard to the sexual nature of the flowers, males, females and hermaphrodites occur in nature, with hermaphroditism being the norm. About 6% of flowering plants are dioecious and 5% monoecious, supporting the widely accepted view that bisexual flowers are the ancestral condition. Unisexuality evolves from hermaphroditism by the process of random mutations affecting the female organ (carpel) or male organ (stamen) abortion. The ABCE model of floral development provides a basic underlying developmental framework of individual floral whorls across species. However, it stops short of universally explaining the occurrence of selective organ abortion, as in the case of unisexual flowers. Abortion of either one of the sexual organs is the first step towards evolving a sexually dimorphic species, mostly by a loss-of-function mutation, rarely by a gain-of-function mutation, occurring in any of a number of genes and regulatory elements involved. Ontogenic similarities between the lateral organ leaf and the flower has also led to research demonstrating increasing roles played by the plant hormone auxin in the initiation and patterning of these organs. Reproductive organs are structurally complex and critical to survival, and have been under intense research for the last three decades. However, the genetic elements and interactions between that sculpt the organs are relatively poorly understood, and neither of these models sufficiently explain the occurrence of different sex types in plants. Stable dioecy results when the two functional genes affecting carpel and stamen development are linked in close proximity and their recessive alleles are linked in repulsion phase. The relatively low frequency of female sterile mutants in nature is indicative of the evolutionary constraints on the female organs by dint of their role in bearing the ovules and providing nutrition and protection to the next generation. It is also caused by the lesser probability of female mutations being fixed in a population as the sedentary recipient nature of carpels would drive the population to extinction. The model plant species Arabidopsis also reflects this dearth of female sterile mutants in laboratory studies. Being a hermaphrodite species with perfect flowers, and with a fully sequenced genome, Arabidopsis is ideally suited to study floral organ development. Carica papaya variety AU9 is an improved dioecious variety with male and female sex types controlled by a pair of nascent sex chromosomes, and with a sequenced genome. It makes for an ideal system to study the underlying genetic basis for floral sex organ development. Arabidopsis and papaya are both in the order Brassicales, with papaya having 2 fewer whole genome duplications than Arabidopsis. To explore and identify genomic regions and gene loci involved in floral organ development, we combined the parallel study of gene expression differences between male and female shoot apical meristem tissue of AU9 with that of sequence analysis of EMS generated female-sterile mutants in Arabidopsis. The combined approach of our study identified a host of gene loci in both papaya and Arabidopsis, and 2 distinct genomic regions in Arabidopsis as putatively involved in the developmental program of the carpels. In papaya, significantly higher number of genes were found to be present in the male tissues compared to the female tissues. Known genes involved in organ development showed a distribution among transcription factors, hormone related functions, transporter proteins, and kinase proteins. We also identified chromatin related proteins which presumably work to maintain genome integrity and accuracy. Of the loci identified to be differentially expressed between males and females, a majority was found to be of unknown function. This was expected as many of the critical regulatory elements function upstream and downstream of the ABCE model and auxin responses are largely uncharacterized. In addition, there should also be crosstalk among effectors of the ABCE class genes and those of the auxin related genes as evident from the combined results of our parallel experiments. A large portion of these gene loci code for proteins containing WD40 repeats, ankyrin repeats, penta-, tetra- and tri- copeptide repeats. Although these protein motifs are found to be involved in a wide variety of physiological functions, emerging evidence of sub-functionalization and additional motif based studies are increasingly implicating them in developmental roles. In our analysis of Arabidopsis mutants, we found genomic regions on the long arms of Chromosome 1 and Chromosome 3 to harbor single nucleotide polymorphisms (SNPs) at a higher frequency and greater density, compared to the rest of the genome. This was an expected situation given that our mutant FS322 displayed a distorted segregation ratio of 15:1, with the mutant phenotype failing to manifest in the second backcross generation. This is suggestive of more than one gene being affected to generate the mutant phenotype. The gene loci identified to be putative candidate genes show a variety of functional roles, and unknown functions. We identified ribosomal structural and functional protein components, F-Box and U-Box proteins, and ankyrin, penta-, tetra- and tri- copeptide repeat containing proteins. The known loci identified to have SNPs include key players such as HUELLENOS (HLL), MEIOSIS DEFECTIVE 1 (MEI1), ESSENTIAL MEIOTIC ENDONUCLEASE 1B (EME 1B), SPATULA (SPT), RIBOSOMAL RNA PROCESSING 5 (RRP5), PRESEQUENCE PROTEASE 1 (PREP1) AND BRASSINOSTEROID-SIGNALING KINASE 2 (BSK2), all of which are known to play roles in female reproductive development.
Issue Date:2017-05-04
Rights Information:Copyright 2017 Setu Chakrabarty
Date Available in IDEALS:2017-09-29
Date Deposited:2017-08

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