Linking Auxin with Photosynthetic Rate via Leaf Venation.

Scott A.M Mcadam,Mary Maconochie,Madeline Carins Murphy,Melanie Best,Peter Mcguiness,Morgane P Eléouët,David S Nichols,Erin L Mcadam,Marion Dalmais,Frances C Sussmilch,Julie M I Hofer,Sam D Cook,Shelley Urquhart,Timothy J Brodribb,John J Ross,Matthew Hegarty,Theodore Dimitriou,Warwick M Gill,Ariane Gélinas-Marion

doi:10.1104/pp.17.00535

Abstract

Land plants lose vast quantities of water to the atmosphere during photosynthetic gas exchange. In angiosperms, a complex network of veins irrigates the leaf, and it is widely held that the density and placement of these veins determines maximum leaf hydraulic capacity and thus maximum photosynthetic rate. This theory is largely based on interspecific comparisons and has never been tested using vein mutants to examine the specific impact of leaf vein morphology on plant water relations. Here we characterize mutants at the Crispoid (Crd) locus in pea (Pisum sativum), which have altered auxin homeostasis and activity in developing leaves, as well as reduced leaf vein density and aberrant placement of free-ending veinlets. This altered vein phenotype in crd mutant plants results in a significant reduction in leaf hydraulic conductance and leaf gas exchange. We find Crispoid to be a member of the YUCCA family of auxin biosynthetic genes. Our results link auxin biosynthesis with maximum photosynthetic rate through leaf venation and substantiate the theory that an increase in the density of leaf veins coupled with their efficient placement can drive increases in leaf photosynthetic capacity.

Highlights

Land plants lose vast quantities of water to the atmosphere during photosynthetic gas exchange
A core body of literature has identified a number of adaptations that reduce the terminal path length for water flow in the leaf and increase Kleaf. These adaptations range from increasing the density of the veins per unit area of leaf (Brodribb et al, 2007; Sack et al, 2013; Caringella et al, 2015), modifying leaf thickness and bundle sheath extensions (Sack et al, 2003; Zsögön et al, 2015) through to the formation of accessory transfusion tissue (Brodribb and Holbrook, 2005), and the formation and placement of free-ending veinlets (FEVs) within areoles
Between the terminal path length for water flow through the mesophyll and maximum Kleaf (Sack and Frole, 2006; Brodribb et al, 2007, 2010; Sack et al, 2013; Scoffoni et al, 2016). These correlations are supported by singlegene vein density mutants in Arabidopsis (Arabidopsis thaliana) and Solanum lycopersicum spanning a spectrum of vein modifications that influence Kleaf (Caringella et al, 2015; Zsögön et al, 2015)

Summary

RESULTS

Homozygous recessive crd mutants are distinguished from wild-type (Swiecicki, 1989; Berdnikov et al, 2000) plants due to a noticeable reduction in vein density (Fig. 1, A and B; Supplemental Table S1). Was expressed in WT-3 samples but showed complete absence of expression in crd-3 mutant samples, consistent with a fast neutron-generated deletion This contig corresponded to the entire last exon and portion of the 39 UTR of PsYUC1, a previously identified pea homolog of AtYUC1/AtYUC4/ PhFLOOZY, encoding a 411-amino acid flavincontaining mono-oxygenase (FMO) protein (Tivendale et al, 2010). In contrast to WT-4 leaves, no GUS staining was observed in young leaves (,4 mm in length) of crd-4 DR5::GUS plants, indicating reduced auxin activity (Supplemental Fig. S9) We further investigated this difference in auxin activity in developing leaves by quantifying the levels of both free IAA and the auxin conjugate, IAA-Asp (IAAsp), in apical tissue containing developing leaves and meristematic tissue. A reduction in free IAA levels was not observed in whole shoots (Supplemental Fig. S10)

DISCUSSION

Findings

MATERIALS AND METHODS