Loss of ancestral function in duckweed roots is accompanied by progressive anatomical reduction and a re-distribution of nutrient transporters
Alexander Ware, Dylan Jones, Paulina Flis, Elina Chrysanthou, Kellie E. Smith, Britta M. C. Kümpers, Levi Yant, Jonathan A. Atkinson, Darren M. Wells, Rahul Bhosale, Anthony Bishopp
Abstract
Organ loss occurs frequently during plant and animal evolution. Sometimes, non-functional organs are retained through evolution. Vestigial organs are defined as genetically determined structures that have lost their ancestral (or salient) function.1Prout T. Observations on structural reduction in evolution.Am. Nat. 1964; 98: 239-249https://doi.org/10.1086/282323Crossref Google Scholar,2Fong D.W. Kane T.C. Culver D.C. Vestigialization and loss of nonfunctional characters.Annu. Rev. Ecol. Syst. 1995; 26: 249-268https://doi.org/10.1146/ANNUREV.ES.26.110195.001341Crossref Google Scholar,3Muller G.B. Vestigial organs and structures.in: Pagel M. Encyclopaedia of Evolution. Oxford University Press., 2002: 1131-1133Google Scholar Duckweeds, an aquatic monocot family, exhibit both these characteristics. They possess a uniquely simple body plan, variably across five genera, two of which are rootless. Due to the existence of closely related species with a wide diversity in rooting strategies, duckweed roots represent a powerful system for investigating vestigiality. To explore this, we employed a panel of physiological, ionomic, and transcriptomic analyses, with the main goal of elucidating the extent of vestigiality in duckweed roots. We uncovered a progressive reduction in root anatomy as genera diverge and revealed that the root has lost its salient ancestral function as an organ required for supplying nutrients to the plant. Accompanying this, nutrient transporter expression patterns have lost the stereotypical root biased localization observed in other plant species. While other examples of organ loss such as limbs in reptiles4Infante C.R. Mihala A.G. Park S. Wang J.S. Johnson K.K. Lauderdale J.D. Menke D.B. Shared enhancer activity in the limbs and phallus and functional divergence of a limb-genital cis-regulatory element in snakes.Dev. Cell. 2015; 35: 107-119https://doi.org/10.1016/J.DEVCEL.2015.09.003Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar or eyes in cavefish5Yamamoto Y. Stock D.W. Jeffery W.R. Hedgehog signalling controls eye degeneration in blind cavefish.Nature. 2004; 431: 844-847https://doi.org/10.1038/nature02864Crossref PubMed Scopus (194) Google Scholar frequently display a binary of presence/absence, duckweeds provide a unique snapshot of an organ with varying degrees of vestigialization in closely related neighbors and thus provide a unique resource for exploration of how organs behave at different stages along the process of loss.