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      Engineering Plant Cell Fates and Functions for Agriculture and Industry

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          Abstract

          Many plant species are grown to enable access to specific organs or tissues, such as seeds, fruits, or stems. In some cases, a value is associated with a molecule that accumulates in a single type of cell. Domestication and subsequent breeding have often increased the yields of these target products by increasing the size, number, and quality of harvested organs and tissues but also via changes to overall plant growth architecture to suit large-scale cultivation. Many of the mutations that underlie these changes have been identified in key regulators of cellular identity and function. As key determinants of yield, these regulators are key targets for synthetic biology approaches to engineer new forms and functions. However, our understanding of many plant developmental programs and cell-type specific functions is still incomplete. In this Perspective, we discuss how advances in cellular genomics together with synthetic biology tools such as biosensors and DNA-recording devices are advancing our understanding of cell-specific programs and cell fates. We then discuss advances and emerging opportunities for cell-type-specific engineering to optimize plant morphology, responses to the environment, and the production of valuable compounds.

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          Most cited references59

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          Genomic analyses provide insights into the history of tomato breeding.

          The histories of crop domestication and breeding are recorded in genomes. Although tomato is a model species for plant biology and breeding, the nature of human selection that altered its genome remains largely unknown. Here we report a comprehensive analysis of tomato evolution based on the genome sequences of 360 accessions. We provide evidence that domestication and improvement focused on two independent sets of quantitative trait loci (QTLs), resulting in modern tomato fruit ∼100 times larger than its ancestor. Furthermore, we discovered a major genomic signature for modern processing tomatoes, identified the causative variants that confer pink fruit color and precisely visualized the linkage drag associated with wild introgressions. This study outlines the accomplishments as well as the costs of historical selection and provides molecular insights toward further improvement.
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            The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1.

            Vegetative and reproductive phases alternate regularly during sympodial growth in tomato. In wild-type 'indeterminate' plants, inflorescences are separated by three vegetative nodes. In 'determinate' plants homozygous for the recessive allele of the SELF-PRUNING (SP) gene, sympodial segments develop progressively fewer nodes until the shoot is terminated by two consecutive inflorescences. We show here that the SP gene is the tomato ortholog of CENTRORADIALIS and TERMINAL FLOWER1, genes which maintain the indeterminate state of inflorescence meristems in Antirrhinum and Arabidopsis respectively. The sp mutation results in a single amino acid change (P76L), and the mutant phenotype is mimicked by overexpressing the SP antisense RNA. Ectopic and overexpression of the SP and CEN transgenes in tomato rescues the 'indeterminate' phenotype, conditions the replacement of flowers by leaves in the inflorescence and suppresses the transition of the vegetative apex to a reproductive shoot. The SELF-PRUNING gene is expressed in shoot apices and leaves from very early stages, and later in inflorescence and floral primordia as well. This expression pattern is similar to that displayed by the tomato ortholog LEAFY and FLORICAULA. Comparison of the sympodial, day-neutral shoot system of tomato and the monopodial, photoperiod-sensitive systems of Arabidopsis and Antirrhinum suggests that flowering genes that are required for the processing of floral induction signals in Arabidopsis and Antirrhinum are required in tomato to regulate the alternation between vegetative and reproductive cycles in sympodial meristems.
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              The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability.

              Observed phenotypic variation in the lateral root branching density (LRBD) in maize (Zea mays) is large (1-41 cm(-1) major axis [i.e. brace, crown, seminal, and primary roots]), suggesting that LRBD has varying utility and tradeoffs in specific environments. Using the functional-structural plant model SimRoot, we simulated the three-dimensional development of maize root architectures with varying LRBD and quantified nitrate and phosphorus uptake, root competition, and whole-plant carbon balances in soils varying in the availability of these nutrients. Sparsely spaced (less than 7 branches cm(-1)), long laterals were optimal for nitrate acquisition, while densely spaced (more than 9 branches cm(-1)), short laterals were optimal for phosphorus acquisition. The nitrate results are mostly explained by the strong competition between lateral roots for nitrate, which causes increasing LRBD to decrease the uptake per unit root length, while the carbon budgets of the plant do not permit greater total root length (i.e. individual roots in the high-LRBD plants stay shorter). Competition and carbon limitations for growth play less of a role for phosphorus uptake, and consequently increasing LRBD results in greater root length and uptake. We conclude that the optimal LRBD depends on the relative availability of nitrate (a mobile soil resource) and phosphorus (an immobile soil resource) and is greater in environments with greater carbon fixation. The median LRBD reported in several field screens was 6 branches cm(-1), suggesting that most genotypes have an LRBD that balances the acquisition of both nutrients. LRBD merits additional investigation as a potential breeding target for greater nutrient acquisition. © 2014 American Society of Plant Biologists. All Rights Reserved.
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                Author and article information

                Journal
                ACS Synth Biol
                ACS Synth Biol
                sb
                asbcd6
                ACS Synthetic Biology
                American Chemical Society
                2161-5063
                04 April 2024
                19 April 2024
                : 13
                : 4
                : 998-1005
                Affiliations
                []Engineering Biology, Earlham Institute , Norwich Research Park, Norwich, NR4 7UZ United Kingdom
                []Department of Plant Sciences, University of Cambridge , Downing Street, Cambridge, CB2 3EA United Kingdom
                Author notes
                Author information
                https://orcid.org/0000-0001-8106-4329
                https://orcid.org/0000-0002-8389-1851
                https://orcid.org/0000-0002-1185-5421
                Article
                10.1021/acssynbio.4c00047
                11036505
                38573786
                0fd47176-d8e4-40dd-a116-bf3256be892e
                © 2024 The Authors. Published by American Chemical Society

                Permits the broadest form of re-use including for commercial purposes, provided that author attribution and integrity are maintained ( https://creativecommons.org/licenses/by/4.0/).

                History
                : 25 January 2024
                : 22 March 2024
                : 21 March 2024
                Funding
                Funded by: UK Research and Innovation, doi 10.13039/100014013;
                Award ID: BB/W014173/1
                Funded by: Biotechnology and Biological Sciences Research Council, doi 10.13039/501100000268;
                Award ID: BBX011070/1
                Funded by: Biotechnology and Biological Sciences Research Council, doi 10.13039/501100000268;
                Award ID: BBS/E/ER/230001C
                Funded by: UK Research and Innovation, doi 10.13039/100014013;
                Award ID: BB/Y007751/1
                Categories
                Perspective
                Custom metadata
                sb4c00047
                sb4c00047

                Molecular biology
                Molecular biology

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