A role for SPEECHLESS in the integration of leaf stomatal patterning with the growth vs disease trade‐off in poplar

Abstract

Occurrence of stomata on both leaf surfaces (amphistomaty) promotes higher stomatal conductance and photosynthesis while simultaneously increasing exposure to potential disease agents in black cottonwood (Populus trichocarpa).A genome-wide association study (GWAS) with 2.2M single nucleotide polymorphisms generated through whole-genome sequencing found 280 loci associated with variation in adaxial stomatal traits, implicating genes regulating stomatal development and behavior. Strikingly, numerous loci regulating plant growth and response to biotic and abiotic stresses were also identified.The most significant locus was a poplar homologue of SPEECHLESS (PtSPCH1). Individuals possessing PtSPCH1 alleles associated with greater adaxial stomatal density originated primarily from environments with shorter growing seasons (e.g. northern latitudes, high elevations) or with less precipitation. PtSPCH1 was expressed in developing leaves but not developing stem xylem. In developing leaves, RNA sequencing showed patterns of coordinated expression between PtSPCH1 and other GWAS-identified genes.The breadth of our GWAS results suggests that the evolution of amphistomaty is part of a larger, complex response in plants. Suites of genes underpin this response, retrieved through genetic association to adaxial stomata, and show coordinated expression during development. We propose that the occurrence of amphistomaty in P. trichocarpa involves PtSPCH1 and reflects selection for supporting rapid growth over investment in immunity.Dedication. We would like to dedicate this manuscript in memory of Carl J. Douglas for his significant contributions in understanding poplar biology and his scientific leadership on the Genome Canada 'POPCAN: Genetic improvement of poplar trees as a Canadian bioenergy feedstock' project.

Hybridization disrupts growth-defense strategies and reveals trade-offs masked in unadmixed populations of a perennial plant

“…The results from this study support theoretical conclusions that the costs of amphistomy are sufficiently high to constrain the available trait space in which plants evolve, and selection from pathogens likely induces a cost of amphistomy that is paid in the currency of fitness. Amphistomy is rare in P. balsamifera , which likely reflects the evolution of fitness optima that prioritizes defense over growth, which stands in contrast to northern populations of P. trichocarpa that have possibly evolved increase stomatal ratio to favor growth over defense (McKown et al, 2014; McKown et al, 2019).…”

“…We conducted a common garden study with naturally formed Populus hybrids to observe how hybridization alters trait value distributions, heritable variation, and the potential to reveal trade-offs and selection conflicts. We focused on growth, disease, and the stomatal ratio, as these traits contribute to fitness and were previously implicated in disease variation within unadmixed P. trichocarpa (McKown et al, 2014; McKown et al, 2019). These results indicate hybridization increases disease severity, decreases growth of hybrids formed from within- Tacamahaca crosses, and increases the stomatal ratio.…”

“…Depending on pathogen prevalence, plant life histories generally evolve towards increased investment in defensive enzymes and compounds paired with slower growth, or decreased investment in defense paired with faster growth. The fast-slow trade-off has been consistently identified in annuals (Tian et al, 2003), perennials (Messina et al, 2002), and long-lived trees (McKown et al, 2014; McKown et al, 2019), although this hypothesis is not without its critics (Kliebenstein, 2016).…”

Stomatal development in the grasses: lessons from models and crops (and crop models)

“…It is also possible to consider candidate genes from QTL and GWAS studies. Genetic studies in tomato and poplar, respectively, suggest that adaxial/abaxial stomatal patterning may be a trait that has been subject to evolutionary selection for specific ecosystems (Muir et al, 2014;McKown et al, 2019). QTL mapping in wild tomato species found a SPCH homologue within the major large-effect locus for stomatal ad/abaxial patterning.…”

Emerging roles for carbonic anhydrase in mesophyll conductance and photosynthesis

“…In a RNA sequencing analysis we compared the expression of eight α‐CAs, three β‐CAs, five γ‐CAs and five unassigned CAs from developing leaves and stem xylem in P. trichocarpa (methodology described in McKown et al , ) using a sequencing library available in the Sequence Read Archive (NCBI SRA) under project #300564 (http://www.ncbi.nlm.nih.gov/bioproject/300564). Sequences were mapped to the P. trichocarpa v.3.0 reference genome.…”